The Journal of Pathology
© (2013) Pathological Society of Great Britain and Ireland
Edited By: Peter A Hall, Editor-in-Chief
Impact Factor: 6.318
ISI Journal Citation Reports © Ranking: 2011: 3/79 (Pathology); 20/196 (Oncology)
Online ISSN: 1096-9896
Welcome to The Journal of Pathology's Virtual Issues page
List of issues
2012 Issue 1, February: Recent advances in our understanding of gynaecological pathology
2011 Issue 4, November: Progress in our understanding of the pathobiology of hypoxia and angiogenesis
2011 Issue 3, August: The molecular pathology of sarcomas
2011 Issue 2, April: Recent advances in the molecular pathology of micro-RNAs
2011 Issue 1, February: Neuropathology: Advances in technology and biology
2010 Issue 4, December: Recent advances in the pathobiology of lymphoma
2010 Issue 3, September: Recent advances in renal pathology
2010 Issue 2, June: Recent advances in breast cancer
2010 Issue 1, April: p53: Recent advances in our understanding of this key tumour suppressor
The Journal of Pathology 2013 Virtual Issue Number 1, February
The microenvironment and cancer
Compiled and annotated by Philip Coates, Dundee Cancer Centre, University of Dundee, Ninewells Hospital and Medical School, Dundee, UK
For many years, the emphasis in cancer research has been to identify genetic changes that occur to oncogenes and tumour suppressor genes during neoplastic initiation and progression. This continues apace, particularly with the ability of next generation sequencing to provide comprehensive analysis of cancer cell genomes. Although this approach has provided many advances, it is clear that the pathobiology of human cancers cannot be explained solely by genetic alterations to the cancer cell: their environment is also critical.
The idea that the microenvironment is important for tumour growth stems back to the work of Paget towards the end of the 19th century in what is generally termed the “seed and soil” hypothesis, where metastatic cells require the appropriate “soil” (or environment) to allow them to “seed” in a distant site. Allied to this proposal is the idea that primary cancers also rely on appropriate environmental cues for survival and growth. The Journal of Pathology has published a variety of research papers, commentaries and reviews in this field that contribute to our understanding of the role of the microenvironment in cancer.
This Virtual Issue highlights some of these recent publications. These papers are now freely available online through this Virtual Issue. In addition, there is a series of questions that can be used within the Royal College of Pathologists Continuing Professional Development (CPD) scheme.
Immune Cells in the Cancer Microenvironment
Tumours both respond to their environment and modify their environment. Tumour-associated macrophages (TAMs) play important roles in maintaining cancer cell growth, reviewed by Alberto Mantovani and colleagues . Similarly, cancer cells secrete cytokines and chemokines for recruiting and modifying macrophages and other leukocytes, a subject reviewed recently by Francis Balkwill . The engulfment of apoptotic tumour cells is an alternative modifier of TAM phenotypes, and is reviewed by Gregory and Pound .
|1|| Macrophage plasticity and polarization in tissue repair and remodelling|
Alberto Mantovani, Subhra K. Biswas, Maria Rosaria Galdiero, Antonio Sica and Massimo Locati
The Journal of Pathology 2013;229:176-185. (Review)
|2|| The chemokine system and cancer|
Frances R Balkwill
The Journal of Pathology 2012 Jan;226(2):148-57. (Review)
Cell death in the neighbourhood: direct microenvironmental effects of apoptosis in normal and neoplastic tissues
Several recent original research papers highlight the roles of innate immune cells in cancer. In the first, macrophage ablation in an experimental skin cancer model reduced angiogenesis, tumour growth and invasion. 2 Macrophage recruitment was stimulated by VEGF and polarization into M2 cells was caused by IL-4 and IL-10, produced, respectively, by the tumour cells and macrophages themselves , discussed in an accompanying commentary . Two studies implicate neutrophils in promoting metastasis. In the first, hyaluronan fragments produced by tumour cells activate neutrophils through TLR4 and educate them to adopt a phenotype that stimulates metastasis. Importantly, neutrophil accumulation is seen in the stroma of cervical, colorectal, hepatocellular and gastric carcinomas, although neutrophil accumulation correlated with metastasis only in the latter two tumours . In the second study, a novel system was developed using transparent zebrafish inoculated with tumour cells. Neutrophil migration was shown to control invasion by conditioning the collagen matrix to form the metastatic “soil”  and this model is likely to be useful for other studies of the metastatic process .
|4|| Vascular endothelial growth factor-induced skin carcinogenesis depends on recruitment and alternative activation of macrophages|
Nina Linde, Wiltrud Lederle, Sofia Depner, Nico van Rooijen, Claudia M Gutschalk and Margareta M Mueller
The Journal of Pathology 2012;227:17-28. (Original paper)
|5|| Partners in crime: VEGF and IL-4 conscript tumour-promoting macrophages|
Michele De Palma
The Journal of Pathology 2012;227:4-7.
|6|| Neutrophils promote motility of cancer cells via a hyaluronan-mediated TLR4/PI3K activation loop|
Yan Wu, Qiyi Zhao, Chen Peng, Lin Sun, Xue-Feng Li and Dong-Ming Kuang
The Journal of Pathology 2011;225:438-47. (Original paper)
|7|| Neutrophil-mediated experimental metastasis is enhanced by VEGFR inhibition in a zebrafish xenograft model|
Shuning He, Gerda EM Lamers, Jan-Willem M Beenakker, Chao Cui, Veerander PS Ghotra, Erik HJ Danen, Annemarie H Meijer, Herman P Spaink and B Ewa Snaar-Jagalska
The Journal of Pathology 2012;227:431-45. (Original paper)
|8|| Live imaging in zebrafish reveals neu(trophil) insight into the metastatic niche|
E Elizabeth Patton
The Journal of Pathology 2012;227:381-4.
In addition to the roles of innate immune system cells, the adaptive immune system is also an important component of the tumour microenvironment, with the preferential recruitment of CD8 T-cells into tumour areas by specific type-1 chemokines indicating the prognostic influence of an inflammatory environment in Ewing sarcoma . Similarly, the ratio of CD8/FOXP3 cells that accumulate after therapy is a predictor of survival . On the other hand, development of metastasis may be independent of the adaptive immune system  and the field of cancer immunoediting was revisited in a recent commentary .
|9|| Pro-inflammatory chemokine-chemokine receptor interactions within the Ewing sarcoma microenvironment determine CD8(+) T-lymphocyte infiltration and affect tumour progression|
Dagmar Berghuis, Susy J Santos, Hans J Baelde, Antonie HM Taminiau, R Maarten Egeler, Marco W Schilham, Pancras CW Hogendoorn and Arjan C Lankester
The Journal of Pathology 2011;223:347-57. (Original paper)
|10|| In situ immune response after neoadjuvant chemotherapy for breast cancer predicts survival|
Sylvain Ladoire, Grégoire Mignot, Sandrine Dabakuyo, Laurent Arnould, Lionel Apetoh, Cedric Rébé, Bruno Coudert, Francois Martin, Marie Hélène Bizollon, André Vanoli, Charles Coutant, Pierre Fumoleau, Franck Bonnetain and François Ghiringhelli
The Journal of Pathology 2011;224:389-400. (Original paper)
|11|| Development of metastatic HER2(+) breast cancer is independent of the adaptive immune system|
Metamia Ciampricotti, Kim Vrijland, Cheei-Sing Hau, Tea Pemovska, Chris W Doornebal, Ewoud N Speksnijder, Katharina Wartha, Jos Jonkers and Karin E de Visser
The Journal of Pathology 2011;224:56-66. (Original paper)
Revisiting cancer immunoediting by understanding cancer immune complexity
Fibroblasts and ECM
Many studies have indicated that fibroblasts found in association with tumour cells have different properties than the corresponding normal tissue fibroblasts [13,14]. Although these properties can be maintained following isolation and culture, the original findings that there may be genetic mutations in these fibroblasts are unlikely . Various studies have also indicated that stromal features and fibroblast gene expression profiles influence progression and mortality in at least some cancers [16,17], with a direct role for caveolin-1 in breast cancer cell invasion .
|13|| From sentinel cells to inflammatory culprits: cancer-associated fibroblasts in tumour-related inflammation|
Charlotte Servais and Neta Erez
The Journal of Pathology 2013;229(2): 198-207. (Review)
|14|| Jekyll and Hyde: the role of the microenvironment on the progression of cancer|
Michael Allen and J Louise Jones
The Journal of Pathology 2011;223:162-76. (Review)
|15|| Genetic changes in tumour microenvironments|
Ian Campbell, Wen Qiu and Izhak Haviv
The Journal of Pathology 2011;223:450-8. (Review)
|16|| Stromal features are predictive of disease mortality in oral cancer patients|
Daniel Marsh, Krishna Suchak, Karwan A Moutasim, Sabarinath Vallath, Colin Hopper, Waseem Jerjes, Tahwinder Upile, Nicholas Kalavrezos, Shelia M Violette, Paul H Weinreb, Kerry A Chester, Jagdeep S Chana, John F Marshall, Ian R Hart, Allan K Hackshaw, Kim Piper and Gareth J Thomas
The Journal of Pathology 2011;223:470-81. (Original paper)
|17|| Fibroblast gene expression profile reflects the stage of tumour progression in oral squamous cell carcinoma|
Kue Peng Lim, Nicola Cirillo, Yazan Hassona, Wenbin Wei, Johanna K Thurlow, Sok Ching Cheong, Gayani Pitiyage, E Ken Parkinson and Stephen S Prime
The Journal of Pathology 2011;223:459-69. (Original paper)
|18|| Clinical and functional significance of loss of caveolin-1 expression in breast cancer-associated fibroblasts|
Samantha A Simpkins, Andrew M Hanby, Deborah L Holliday and Valerie Speirs
The Journal of Pathology 2012;227:490-8. (Original paper)
The following questions can be answered by reading and reflecting upon the above annotation and the papers that are cited within it. Within the Royal College of Pathologists Continuing Professional Development (CPD) scheme, CPD points may be earned by writing reflective notes on the papers in this Virtual Issue and the questions are designed to act as a focus for this activity. To do this, you may wish to use the Royal College of Pathologists' reflective notes form.
|Question 1||Outline the major phenotypes of tumour-associated macrophages and how these help to promote tumour growth and survival|
|Question 2||Outline the general concept of immunoediting and how this is avoided by cancer cells|
|Question 3||Discuss the changes to fibroblasts in the tumour environment and how these changes occur|
The Journal of Pathology 2012 Virtual Issue Number 4, December
Animal models of disease
Compiled and annotated by Richard Poulsom, Blizard Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London, UK
Properly regulated and controlled experimental studies of animal models have the potential to increase our understanding of disease; for example, the effects of careful engineering of a single gene can be assessed in vivo, where responses are subject to the full range of complex interactions normally present. Such studies, despite not being perfect copies of human disease, deliver knowledge with the potential to transform our understanding of the basis of specific pathologies, and for some may point the way for devising and testing therapeutic interventions. Knowledge of the way systems interact over time cannot easily be gained from ‘snapshot’ analysis of human tissues, or cell cultures in vitro, although these too have important roles to play.
The support of government and national funding bodies for ethical frameworks for research involving animals helps ensure in the UK that researchers are aware of their obligations to the principle of the 3Rs (Replacement, Refinement and Reduction). We make reference to this in our author guidelines (see Author guidelines section 4.11).
This Virtual Issue of The Journal of Pathology seeks to highlight recent publications that reveal how careful use of animal models particularly in zebrafish and mouse has generated new understanding in three areas of disease.
The zebrafish is increasingly useful for generating models of disease and an Invited Review article explains how zebrafish offer new insights into cardiovascular genetics and drug discovery screening . A porcine model of myocardial ischaemia/reperfusion injury was used to test the involvement of Early-growth response-1 (Egr-1) in driving myocardial damage; intracoronary-administration of DNAzymes that targeted human EGR-1 sequences were effective at reducing Egr-1 mRNA and protein in cardiomyocytes in the area at risk, and attenuating levels of the pro-coagulant and pro-inflammatory molecule PAI-1 . An update on Egr-1 and its role in orchestrating fibrosis features in our 2013 Annual Review Issue . Transgenic mice were used to help understand what drives the fibrotic remodelling seen in chronic rejection of transplanted hearts ; mice engineered to prevent expression of a particular splice-variant of fibronectin (EDA cellular fibronectin; ED-A(+) fibronectin) did not develop chronic rejection of wild type allografted hearts even though passing through an acute rejection phase. One implication of this study is that this splice variant, known to be crucial for the development of myofibroblasts within hearts suffering rejection , may offer a therapeutic target for ameliorating fibrosis associated with chronic cardiac allograft rejection.
|1||The genetics of cardiovascular disease: new insights from emerging approaches|
Timothy JA Chico, Marta Milo, David C Crossman
The Journal of Pathology 2010; 220:186-197. (Invited review)
|2||Intracoronary delivery of DNAzymes targeting human EGR-1 reduces infarct size following myocardial ischaemia reperfusion|
Ravinay Bhindi, Roger G Fahmy, Aisling C McMahon, Levon M Khachigian, Harry C Lowe
The Journal of Pathology 2012; 227: 157-164. (Original paper)
|3||Egr-1: a new conductor for the fibrosis orchestra|
Swati Bhattacharyya, Feng Fang, Warren Tourtellotte, John Varga
The Journal of Pathology 2013; DOI: 10.1002/path.4131 (Invited review)
|4||Recipient-derived EDA fibronectin promotes cardiac allograft fibrosis|
Adam J Booth, Sherri C Wood, Ashley M Cornett, Alyssa A Dreffs, Guanyi Lu, Andrés F Muro, Eric S White, D Keith Bishop
The Journal of Pathology 2012; 226: 609-618. (Original paper)
|5||Chronic cardiac allograft rejection: critical role of ED-A plus fibronectin and implications for targeted therapy strategies|
Marcus Franz, Dario Neri, Alexander Berndt
The Journal of Pathology 2012; 226: 557-561. (Commentary)
Xenografting cancer cell lines into immunocompromised host mice is one way to assess, and potentially interfere with, invasive and metastatic behaviours in vivo. There are concerns that the process of establishing a cell line that does well in vitro selects for particular phenotypes and genotypes and may not accurately represent the original tumour. Grisanzio and colleagues  sought to avoid such problems by assessing the morphological, phenotypic and genetic characteristics of primary renal cell carcinomas (RCC) and the tumours that grew from them when small pieces were allografted beneath the renal capsules of mice. Serial allografting could offer animal models that closely resemble patient RCC in patients and allow more relevant in vivo preclinical drug testing. A simple immunohistochemical test that could help screen for predisposition to hereditary leiomyoma and renal cell carcinoma (HLRCC) was recently described. The test detects proteins that have been aberrantly succinated following the accumulation of fumarate resulting from blockage of the Krebs cycle by mutation of FH in humans or Fh1 in mice .
|6||Orthotopic xenografts of RCC retain histological, immunophenotypic and genetic features of tumours in patients|
Chiara Grisanzio, Apryle Seeley, Michelle Chang, Michael Collins, Arianna Di Napoli, Su-Chun Cheng, Andrew Percy, Rameen Beroukhim, Sabina Signoretti
The Journal of Pathology 2011; 225: 212-221. (Original paper)
|7||Aberrant succination of proteins in fumarate hydratase-deficient mice and HLRCC patients is a robust biomarker of mutation status|
Chiara Bardella, Mona El-Bahrawy, Norma Frizzell, Julie Adam, Nicola Ternette, Emine Hatipoglu, Kimberley Howarth, Linda O'Flaherty, Ian Roberts, Gareth Turner, Jennifer Taylor, Konstantinos Giaslakiotis, Valentine M Macaulay, Adrian L Harris, Ashish Chandra, Heli J Lehtonen, Virpi Launonen, Lauri A Aaltonen, Christopher W Pugh, Radu Mihai, David Trudgian, Benedikt Kessler, John W Baynes, Peter J Ratcliffe, Ian P Tomlinson, Patrick J Pollard
The Journal of Pathology 2011; 225: 4–11. (Original paper)*
Mouse models feature strongly in studies aiming to unravel the involvement of signalling pathways and the precise molecular interactions that contribute to tumour phenotype. Individuals with Peutz-Jeghers syndrome (a rare disorder that develops in individuals with germ line mutation of a threonine kinase; LKB1) develop a gastrointestinal polyposis that was modelled in mice. When expression profiles of human and mouse polyps were compared, activation of non-canonical Wnt signalling through increased levels of Wnt5a was found. In situ hybridisation revealed this occured principally in stromal cells within polyps of both man and mouse . Familial adenomatous polyposis in man results from mutations in APC, and most sporadic colorectal adenocarcinomas also carry APC mutations. The Apcmin+/- mouse develops many small bowel, plus a few large bowel, adenomas, and is studied extensively as a model of tumorigenesis. APC is a large multi-functional protein, but the relative importance of the central versus C-terminal domains has been unclear because usually both are lost by truncating mutations. Tomlinson’s group engineered mice to express a version of Apc that omitted the central core (bearing β-catenin binding and SAMP repeats) and one that produced Apc truncated at the position most commonly mutated in human adenomas – surprisingly the C-terminus of Apc had no discernable effect on adenoma frequency, location or degree of dysplasia . Contrasting with the lack of observable importance of a large part of Apc, mono-allelic missense changes in the tumour suppressor gene FBXW7 frequently result from mutations that do not inactivate the protein but alter specific arginine resides that are involved in substrate recognition and binding. Mice carrying a copy of one such allele Fbxw7R482Q reveal significant effects in lung development , and it was hypothesised that the spectrum of mutations in FBXW7 are selected for because of the specific interactions that are perturbed.
|8||Elevation of WNT5A expression in polyp formation in Lkb1+/- mice and Peutz-Jeghers syndrome|
Cecilia Lai, James Robinson, Sue Clark, Gordon Stamp, Richard Poulsom, Andrew Silver
The Journal of Pathology 2011; 223: 584-592. (Original paper)
|9||The C-terminus of Apc does not influence intestinal adenoma development or progression|
Annabelle Lewis, Hayley Davis, Maesha Deheragoda, Patrick Pollard, Emma Nye, Rosemary Jeffery, Stefania Segditsas, Philip East, Richard Poulsom, Gordon Stamp, Nicholas Wright, Ian Tomlinson
The Journal of Pathology 2012; 226: 73-83. (Original paper)
|10||FBXW7 mutations typically found in human cancers are distinct from null alleles and disrupt lung development|
Hayley Davis, Annabelle Lewis, Bradley Spencer-Dene, Hilda Tateossian, Gordon Stamp, Axel Behrens, Ian Tomlinson
The Journal of Pathology 2011; 224: 180–189. (Original paper)*
Ectopic expression of the RAF1 oncogene is frequently seen in hepatocellular carcinomas (HCC). The effects of an inducibly-expressed mutated form (ΔRaf1) on the transcriptome were explored in a zebrafish liver cell line both in vitro and after grafting into zebrafish embryos. The conservation of basic signalling pathways between zebrafish and man is such that a set of 57 genes were found induced by ΔRaf1 activation in ZFL–ΔRaf1–ER cells, in carcinogen-induced zebrafish liver tumours and in human HCC, along with newly identified transcript of unknown function that might drive early steps towards HCC .
|11||A Delta Raf1-ER-inducible oncogenic zebrafish liver cell model identifies hepatocellular carcinoma signatures|
Shuning He, SF Gabby Krens, Huiqing Zhan, Zhiyuan Gong, Pancras CW Hogendoorn, Herman P Spaink, B Ewa Snaar-Jagalska
The Journal of Pathology 2011; 225: 19-28. (Original paper)*
Vascularisation is an important step supporting tumour growth that is supported frequently by the expression of Vascular Endothelial Growth Factor (VEFGA) by tumours. Ectopic expression of Vegfa in a non-tumourigenic human keratinocyte cell line was sufficient to induce malignant growth supported by extensive vascularisation via a mechanism requiring influx of macrophages (by chemotaxis to Vegfa) that became M2-polarised by locally produced IL-4 and IL-10. Growth of subcutaneous or surface grafted Vegfa-expressing keratinocytes and invasion of endothelial cells was reduced by depletion of body macrophages, or blockade of IL-4R . New vessels growing into tumours often feature aberrant vessel morphology and function [12, 13]. One factor affecting this is β3 integrin, as revealed by studies of tumour growth in mice that have received bone marrow from either wild type or β3 integrin-null donor mice. Mice receiving bone marrow grafts that cannot express β3 integrin exhibit enhanced mobilisation of endothelial precursors in response to Vegfa and a stronger angiogenic response to tumours, but this is accompanied by reduced functionality of the new tumour blood vessels .
|12||Vascular endothelial growth factor-induced skin carcinogenesis depends on recruitment and alternative activation of macrophages|
Nina Linde, Wiltrud Lederle, Sofia Depner, Nico van Rooijen, Claudia M Gutschalk, Margareta M Mueller
The Journal of Pathology 2012; 227: 17-28. (Original paper)
|13||Deficiency of bone marrow β3-integrin enhances non-functional neovascularization|
Alan R Watson, Simon C Pitchford, Louise E Reynolds, Natalie Direkze, Mairi Brittan, Malcolm R Alison, Sara Rankin, Nicholas A Wright, Kairbaan M Hodivala-Dilke
The Journal of Pathology 2010; 220: 435-445. (Original paper)
Studying what happens when circulating tumour cells enter tissues potentially to establish a metastasis has been made possible in a transparent zebrafish model that allows direct observation of fluorescently marked exogenous and endogenous cells in vivo. This revealed the involvement of neutrophils in establishing a metastatic niche by leaving trails through extracellular matrices. Another important observation was that VEGFR inhibition increased tumour cell invasion even though reducing tumour vascularisation [14, 15]. Zebrafish have also been used as recipients of mouse osteosarcoma-producing cells and progenitor mouse mesenchymal stem cells (MSC). Only the transformed cells migrated through the zebrafish embryo and induced angiogenesis. Whole genome expression analysis of the mouse cells and the zebrafish hosts was carried out to see what influenced behaviour, and pointed to the specific induction of two genes in transformed mouse MSC and suppression of zebrafish immune response-related genes .
|14||Neutrophil-mediated experimental metastasis is enhanced by VEGFR inhibition in a zebrafish xenograft model|
Shuning He, Gerda EM Lamers, Jan-Willem M Beenakker, Chao Cui, Veerander PS Ghotra, Erik HJ Danen, Annemarie H Meijer, Herman P Spaink, B Ewa Snaar-Jagalska
The Journal of Pathology 2012; 227: 431-445. (Original paper)
|15||Live imaging in zebrafish reveals neu(trophil) insight into the metastatic niche|
The Journal of Pathology 2012; 227: 381-384. (Commentary)
|16||An osteosarcoma zebrafish model implicates Mmp-19 and Ets-1 as well as reduced host immune response in angiogenesis and migration|
Alexander B Mohseny, Wei Xiao, Ralph Carvalho, Herman P Spaink, Pancras CW Hogendoorn, Anne-Marie Cleton-Jansen
The Journal of Pathology 2012; 227: 245-253. (Original paper)
Extracellular matrix pathology
Understanding the non-protein composition of extracellular matrices and how it alters in development and disease is extremely challenging. The zebrafish has received strong support as a model of human skeletal development and associated pathologies from the study of five mutant lines with specific genes affecting proteoglycan composition . Polyethyleneimine was used to stain proteoglycan-rich anionic sites for comparison of zebrafish and human cartilaginous structures .
|17||Cartilage ultrastructure in proteoglycan-deficient zebrafish mutants brings to light new candidate genes for human skeletal disorders|
Malgorzata I Wiweger, Cristina M Avramut, Carlos E de Andrea, Frans A Prins, Abraham J Koster, Raimond BG Ravelli, Pancras CW Hogendoorn
The Journal of Pathology 2011; 223: 531-541. (Original paper)
|18||Growth plate regulation and osteochondroma formation: insights from tracing proteoglycans in zebrafish models and human cartilage|
Carlos E de Andrea, Frans A Prins, Malgorzata I Wiweger, Pancras CW Hogendoorn
The Journal of Pathology 2011; 224: 160-168. (Original paper)
Fibrosis contributes to disease of many types and is a focus of the 2013 Annual Review Issue of The Journal of Pathology. The introductory article sets the scene for a series of Invited Review articles . Elsewhere in The Journal, are reports in which animal models have been used to increase understanding of the involvement of the TGF-β/ALK5/Smad pathway in experimental colitis  and to explore the mechanism by which low doses of the anti-tumour drug paclitaxel reduce tubule-interstitial fibrosis in 5/6 nephrectomised rats by reducing TGF-β–Smad signalling and down-regulating a specific microRNA capable of increasing expression of relevant fibrillar and non-fibrillar collagen mRNAs .
|19||Inflammation, wound repair and fibrosis: reassessing the spectrum of tissue injury and resolution|
Eric S White, Alberto Mantovani
The Journal of Pathology 2013; 229: DOI: 10.1002/path.4126. (Introductory article)
|20||Transforming growth factor-beta type 1 receptor (ALK5) and Smad proteins mediate TIMP-1 and collagen synthesis in experimental intestinal fibrosis|
Carlos Medina, Maria Jose Santos-Martinez, Alfredo Santana, Maria Cristina Paz-Cabrera, Michael J Johnston, Marisabel Mourelle, Antonio Salas, Francisco Guarner
The Journal of Pathology 2011; 224: 461-472. (Original paper)
|21||Low-dose paclitaxel ameliorates fibrosis in the remnant kidney model by down-regulating miR-192|
Lin Sun, Dongshan Zhang, Fuyou Liu, Xudong Xiang, Guanghui Ling, Li Xiao, Yinghong Liu, Xuejing Zhu, Ming Zhan, Yeyi Yang, Vinay K Kondeti, Yashpal S Kanwar
The Journal of Pathology 2011; 225: 364-377. (Original paper)
Note: Original papers marked * were shortlisted for the 2011 Jeremy Jass Prize for Research Excellence in Pathology .
|22||2011 Jeremy Jass Prize for Research Excellence in Pathology|
The Journal of Pathology 2012; 228: 429–430. (Announcement)