Distinct sites of renal fibrosis in Crim1 mutant mice arise from multiple cellular origins

Journal of Pathology

Volumn 229, Issue 5, 2013, Pages 685-696

  Phua, Yu Leng ^a   Martel, Nick ^a   Pennisi, David J ^a   Little, Melissa H ^a   Wilkinson, Lorine ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

collagen type III; Crim1; endothelial cells; endothelial mesenchymal transition; glomerulus; Havcr1 Kim1; monocytes; renal fibrosis; renal inflammation

Indexed keywords

CD31 ANTIGEN; CRIM1 PROTEIN; KIDNEY INJURY MOLECULE 1; MEMBRANE PROTEIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; DISEASE MARKER; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM; ENDOTHELIUM CELL; FIBROGENESIS; GENE EXPRESSION PROFILING; KIDNEY FIBROSIS; KIDNEY TUBULE; MONOCYTE; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; ANTIGENS, CD31; BIOLOGICAL MARKERS; BONE MORPHOGENETIC PROTEIN RECEPTORS; CELL LINEAGE; ENDOTHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENETIC MARKERS; GENOTYPE; INTEGRASES; KIDNEY; KIDNEY DISEASES; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; MONOCYTES; MUTATION; MYOFIBROBLASTS; PHENOTYPE; RECEPTOR PROTEIN-TYROSINE KINASES; RNA, MESSENGER;

EID: 84875053173     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4155     Document Type: Article

References (51)

1. Liu Y., Renal fibrosis: New insights into the pathogenesis and therapeutics. Kidney Int 2006; 69: 213-217.
2. Liu Y., Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J Am Soc Nephrol 2004; 15: 1-12.
3. Lõpez-Novoa JM, Nieto MA,. Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO Mol Med 2009; 1: 303-314.
4. Kalluri R, Neilson EG,. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003; 112: 1776-1784.
5. Iwano M, Plieth D, Danoff TM, et al,. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 2002; 110: 341-350.
6. Guarino M, Tosoni A, Nebuloni M,. Direct contribution of epithelium to organ fibrosis: epithelial-mesenchymal transition. Hum Pathol 2009; 40: 1365-1376.
7. Humphreys BD, Lin S-L, Kobayashi A, et al,. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 2010; 176: 85-97.
8. Zeisberg EM, Potenta SE, Sugimoto H, et al,. Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition. J Am Soc Nephrol 2008; 19: 2282-2287.
9. Li J, Qu X, Bertram JF,. Endothelial-myofibroblast transition contributes to the early development of diabetic renal interstitial fibrosis in streptozotocin-induced diabetic mice. Am J Pathol 2009; 175: 1380-1388.
10. Basile DP, Friedrich JL, Spahic J, et al,. Impaired endothelial proliferation and mesenchymal transition contribute to vascular rarefaction following acute kidney injury. Am J Physiol Renal Physiol 2011; 300: F721-733.
11. Li J, Deane JA, Campanale NV, et al,. The contribution of bone marrow-derived cells to the development of renal interstitial fibrosis. Stem Cells 2007; 25: 697-706.
12. Kisanuki YY, Hammer RE, Miyazaki J-i, et al,. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol 2001; 230: 230-242.
13. Venneri MA, Palma MD, Ponzoni M, et al,. Identification of proangiogenic TIE2-expressing monocytes (TEMs) in human peripheral blood and cancer. Blood 2007; 109: 5276-5285.
14. De Palma M, Venneri MA, Galli R, et al,. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 2005; 8: 211-226.
15. Iurlaro M, Scatena M, Zhu W-H, et al,. Rat aorta-derived mural precursor cells express the Tie2 receptor and respond directly to stimulation by angiopoietins. J Cell Sci 2003; 116: 3635-3643.
16. Brunskill EW, Georgas K, Rumballe B, et al,. Defining the molecular character of the developing and adult kidney podocyte. PLoS ONE 2011; 6: e24640.
17. KST264/KST264 mice implicate Crim1 in the regulation of vascular endothelial growth factor-A activity during glomerular vascular development. J Am Soc Nephrol 2007; 18: 1697-1708.
18. Wilkinson L, Gilbert T, Sipos A, et al,. Loss of renal microvascular integrity in postnatal Crim1 hypomorphic transgenic mice. Kidney Int 2009; 76: 1161-1171.
19. Wilkinson L, Kurniwan ND, Phua YL, et al,. Association between congenital defects in papillary outgrowth and functional obstruction in Crim1 mutant mice. J Pathol 2012; 227: 499-510.
20. KST264/KST264 mice display a disruption of the Crim1 gene resulting in perinatal lethality with defects in multiple organ systems. Dev Dynam 2007; 236: 502-511.
21. de Lange WJ, Halabi CM, Beyer AM, et al,. Germ line activation of the Tie2 and SMMHC promoters causes non-cell-specific deletion of floxed alleles. Physiol Genom 2008; 35: 1-4.
22. Du P, Kibbe WA, Lin SM. lumi: a pipeline for processing Illumina microarray. Bioinformatics 2008; 24: 1547-1548.
23. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Statist Applic Genet Mol Biol 2004; 3: Article 3.
24. Gong P, Canaan A, Wang B, et al,. The ubiquitin-like protein FAT10 mediates NF-κB activation. J Am Soc Nephrol 2010; 21: 316-326.
25. Sheerin NS, Risley P, Abe K, et al,. Synthesis of complement protein C3 in the kidney is an important mediator of local tissue injury. FASEB J 2008; 22: 1065-1072.
26. Kim Y, Peyrol S, So C-K, et al,. Coexpression of the lysyl oxidase-like gene (LOXL) and the gene encoding type III procollagen in induced liver fibrosis. J Cell Biochem 1999; 72: 181-188.
27. Schanstra JP, Bachvarova M, Neau E, et al,. Gene expression profiling in the remnant kidney model of wild-type and kinin B1 and B2 receptor knockout mice. Kidney Int 2007; 72: 442-454.
28. Ko GJ, Grigoryev DN, Linfert D, et al,. Transcriptional analysis of kidneys during repair from AKI reveals possible roles for NGAL and KIM-1 as biomarkers of AKI-to-CKD transition. Am J Physiol Renal Physiol 2010; 298: F1472-1483.
29. Ichimura T, Bonventre JV, Bailly V, et al,. Kidney injury molecule-1 (KIM-1), a putative epithelial cell adhesion molecule containing a novel immunoglobulin domain, is up-regulated in renal cells after injury. J Biol Chem 1998; 273: 4135-4142.
30. Soylemezoglu O, Wild G, Dalley AJ, et al,. Urinary and serum type III collagen: markers of renal fibrosis. Nephrol Dialysis Transpl 1997; 12: 1883-1889.
31. Zeisberg EM, Tarnavski O, Zeisberg M, et al,. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007; 13: 952-961.
32. Xu J, Lamouille S, Derynck R,. TGF-β-induced epithelial to mesenchymal transition. Cell Res 2009; 19: 156-172.
33. Donnahoo KK, Meng X, Ayala A, et al,. Early kidney TNF-α expression mediates neutrophil infiltration and injury after renal ischemia-reperfusion. Am J Physiol Regulat Integ Compar Physiol 1999; 277: R922-929.
34. Schmitt-Graff A, Skalli O, Gabbiani G,. α-Smooth muscle actin is expressed in a subset of bone marrow stromal cells in normal and pathological conditions. Virchows Archiv B Cell Pathol Mol Pathol 1989; 57: 291-302.
35. Liu Y., Cellular and molecular mechanisms of renal fibrosis. Nat Rev Nephrol 2011; 7: 684-696.
36. Li J, Deane JA, Campanale NV, et al,. Blockade of p38 mitogen-activated protein kinase and TGF-β1/Smad signaling pathways rescues bone marrow-derived peritubular capillary endothelial cells in adriamycin-induced nephrosis. J Am Soc Nephrol 2006; 17: 2799-2811.
37. Andrae J, Gallini R, Betsholtz C,. Role of platelet-derived growth factors in physiology and medicine. Genes Dev 2008; 22: 1276-1312.
38. Bonner JC,. Regulation of PDGF and its receptors in fibrotic diseases. Cytokine Growth Factor Rev 2004; 15: 255-273.
39. Salvucci O, de la Luz Sierra M, Martina JA, et al,. EphB2 and EphB4 receptors forward signaling promotes SDF-1-induced endothelial cell chemotaxis and branching remodeling. Blood 2006; 108: 2914-2922.
40. Wagner N, Michiels JF, Schedl A, et al,. The Wilms' tumour suppressor WT1 is involved in endothelial cell proliferation and migration: expression in tumour vessels in vivo. Oncogene 2008; 27: 3662-3672.
41. Scholz H, Wagner KD, Wagner N,. Role of the Wilms' tumour transcription factor, Wt1, in blood vessel formation. Pflügers Archiv Eur J Physiol 2009; 458: 315-323.
42. Miller-Hodges E, Hohenstein P,. WT1 in disease: shifting the epithelial-mesenchymal balance. J Pathol 2012; 226: 229-240.
43. Ichimura T, Asseldonk EJPv, Humphreys BD, et al. Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J Clin Invest 2008; 118: 1657-1668.
44. Martin TA, Harrison GM, Mason MD, et al,. HAVcR-1 reduces the integrity of human endothelial tight junctions. Anticancer Res 2011; 31: 467-473.
45. Bariety J, Hill GS, Mandet C, et al,. Glomerular epithelial-mesenchymal transdifferentiation in pauci-immune crescentic glomerulonephritis. Nephrol Dialysis Transpl 2003; 18: 1777-1784.
46. Ng Y-Y, Fan J-M, Mu W, et al,. Glomerular epithelial-myofibroblast transdifferentiation in the evolution of glomerular crescent formation. Nephrol Dialysis Transpl 1999; 14: 2860-2872.
47. Chevalier R., Molecular and cellular pathophysiology of obstructive nephropathy. Pediatr Nephrol 1999; 13: 612-619.
48. Basile DP, Donohoe D, Roethe K, et al,. Renal ischemic injury results in permanent damage to peritubular capillaries and influences long-term function. Am J Physiol Renal Physiol 2001; 281: F887-F899.
49. Hakroush S, Moeller MJ, Theilig F, et al,. Effects of increased renal tubular vascular endothelial growth factor (VEGF) on fibrosis, cyst formation, and glomerular disease. Am J Pathol 2009; 175: 1883-1895.
50. Chevalier RL,. Perinatal obstructive nephropathy. Semin Perinatol 2004; 28: 124-131.
51. Tarantal AF, Han VKM, Cochrum KC, et al,. Fetal rhesus monkey model of obstructive renal dysplasia. Kidney Int 2001; 59: 446-456.