Biomechanical strain causes maladaptive gene regulation, contributing to alport glomerular disease

Kidney International

Volumn 76, Issue 9, 2009, Pages 968-976

  Meehan, Daniel T ^a   Delimont, Duane ^a   Cheung, Linda ^a   Zallocchi, Marisa ^a   Sansom, Steven C ^b   Holzclaw, J David ^b   Rao, Velidi ^a   Cosgrove, Dominic ^a  

^a BOYS TOWN NATIONAL RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Alport syndrome; Biomechanical strain; Podocyte adhesion

Indexed keywords

GELATINASE B; INTERLEUKIN 6; MATRIX METALLOPROTEINASE 14; N(G) NITROARGININE METHYL ESTER; STROMELYSIN; STROMELYSIN 2;

ALPORT SYNDROME; ANIMAL EXPERIMENT; ARTICLE; BIOMECHANICS; CONTROLLED STUDY; DISEASE COURSE; GENE CONTROL; GLOMERULOPATHY; GLOMERULUS BASEMENT MEMBRANE; HYPERTENSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEINURIA;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BLOOD PRESSURE; CELLS, CULTURED; CYTOSKELETON; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GLOMERULAR BASEMENT MEMBRANE; HYPERTENSION; INTERLEUKIN-6; KIDNEY GLOMERULUS; MATRIX METALLOPROTEINASE 10; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; NEPHRITIS, HEREDITARY; NG-NITROARGININE METHYL ESTER; PODOCYTES; PROTEINURIA; RNA, MESSENGER; SODIUM CHLORIDE, DIETARY; STRESS, MECHANICAL; TIME FACTORS;

EID: 70350074361     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2009.324     Document Type: Article

References (46)

1. Cosgrove DE, Meehan DT, Grunkemeyer JA et al. Collagen COL4A3 knockout: a mouse model for autosomal Alport syndrome. Genes Dev 1996; 10: 2981-2992.
2. Abrahamson DR, Isom K, Roach E et al. Laminin compensation in collagen alpha3(IV) knockout (Alport) glomeruli contributes to permeability defects. J Am Soc Nephrol 2007; 18: 2465-2472.
3. Gunwar S, Ballester F, Noelken ME et al. Glomerular basement membrane. Identification of a novel disulfide-cross-linked network of alpha3, alpha4, and alpha5 chains of type IV collagen and its implications for the pathogenesis of Alport syndrome. J Biol Chem 1998; 273: 8767-8775.
4. Zeisberg M, Khurana M, Rao VH et al. Stage-specific action of matrix metalloproteinases influences progressive hereditary kidney disease. PLoS Med 2006; 3: e100.
5. Rao VH, Meehan DT, Delimont D et al. Role for macrophage metalloelastase in glomerular basement membrane damage associated with Alport syndrome. Am J Pathol 2006; 169: 32-46.
6. Cosgrove D, Meehan DT, Delimont D et al. Integrin a1b1 regulates matrix metalloproteinases via P38 mitogen-activated protein kinase in mesangial cells: implications for Alport syndrome. Am J Pathol 2008; 172: 761-773.
7. Borza CM, Borza DB, Pedchenko V et al. Human podocytes adhere to the KRGDS motif of the alpha3alpha4alpha5 collagen IV network. J Am Soc Nephrol 2008; 19: 677-684.
8. Cummins PM, von Offenberg SN, Killeen MT et al. Cyclic strain-mediated matrix metalloproteinase regulation within the vascular endothelium: a force to be reckoned with. Am J Physiol Heart Circ Physiol 2007; 292: H28-H42.
9. Durvasula RV, Petermann AT, Hiromura K et al. Activation of a local tissue angiotensin system in podocytes by mechanical strain. Kidney Int 2004; 65: 30-39.
10. Durvasula RV, Shankland SJ. Mechanical strain increases SPARC levels in podocytes: implications for glomerulosclerosis. Am J Physiol Renal Physiol 2005; 289: F577-F584.
11. Endlich N, Sunohara M, Nietfeld W et al. Analysis of differential gene expression in stretched podocytes: osteopontin enhances adaptation of podocytes to mechanical stress. FASEB J 2002; 16: 1850-1852.
12. Van Themsche C, Alain T, Kossakowska AE et al. Stromelysin-2 (matrix metalloproteinase 10) is inducible in lymphoma cells and accelerates the growth of lymphoid tumors in vivo. J Immunol 2004; 173: 3605-3611. (Pubitemid 39280719)
13. Andreas K, Lubke C, Haupl T et al. Key regulatory molecules of cartilage destruction in rheumatoid arthritis: an in vitro study. Arthritis Res Ther 2008; 10: R9.
14. Patrie KM, Drescher AJ, Welihinda A et al. Interaction of two actin-binding proteins, synaptopodin and alpha-actinin-4, with the tight junction protein MAGI-1. J Biol Chem 2002; 277: 30183-30190.
15. Asanuma K, Kim K, Oh J et al. Synaptopodin regulates the actin-bundling activity of alpha-actinin in an isoform-specific manner. J Clin Invest 2005; 115: 1188-1198.
16. Asanuma K, Yanagida-Asanuma E, Faul C et al. Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat Cell Biol 2006; 8: 485-491.
17. Bartunek J, Weinberg EO, Tajima M et al. Chronic N(G)-nitro-L-arginine methyl ester-induced hypertension: novel molecular adaptation to systolic load in absence of hypertrophy. Circulation 2000; 101: 423-429.
18. Krege JH, Hodgin JB, Hagaman JR et al. A noninvasive computerized tail-cuff system for measuring blood pressure in mice. Hypertension 1995; 25: 1111-1115.
19. Rheault MN, Kren SM, Thielen BK et al. Mouse model of X-linked Alport syndrome. J Am Soc Nephrol 2004; 15: 1466-1474.
20. Cosgrove D, Kalluri R, Miner JH et al. Choosing a mouse model to study the molecular pathobiology of Alport glomerulonephritis. Kidney Int 2007; 71: 615-618.
21. Hartner A, Cordasic N, Klanke B et al. Strain differences in the development of hypertension and glomerular lesions induced by deoxycorticosterone acetate salt in mice. Nephrol Dial Transplant 2003; 18: 1999-2004.
22. Cosgrove D, Rodgers K, Meehan D et al. Integrin alpha1beta1 and transforming growth factor-beta1 play distinct roles in alport glomerular pathogenesis and serve as dual targets for metabolic therapy. Am J Pathol 2000; 157: 1649-1659.
23. Kashtan CE, Kim Y, Lees GE et al. Abnormal glomerular basement membrane laminins in murine, canine, and human Alport syndrome: aberrant laminin alpha2 deposition is species independent. J Am Soc Nephrol 2001; 12: 252-260.
24. Endlich N, Kress KR, Reiser J et al. Podocytes respond to mechanical stress in vitro. J Am Soc Nephrol 2001; 12: 413-422.
25. Enlich N, Enlich K. Stretch, tension and adhesion-adaptive mechanisms of the actin cytoskeleton in podocytes. Eur J Biochem 2006; 85: 229-234.
26. Lorenzen J, Shah R, Biser A et al. The role of osteopontin in the development of albuminuria. J Am Soc Nephrol 2008; 19: 884-890.
27. Brennar BM. Nephron adaptation to renal injury orablation. Am J Physiol 1985; 249: F324-F337.
28. Park CH, Lee MJ, Ahn J et al. Heat shock-induced matrix metalloproteinase (MMP)-1 and MMP-3 are mediated through ERK and JNK activation via an autocrine interleukin-6 loop. J Invest Dermatol 2004; 123: 1012-1019.
29. Van Themsche C, Alain T, Kossakowska AE et al. Sromelysin-2 (matrix metalloproteinase 10)is inducible in lymphoma cells and accelerates the growth of lymphoid tumors in vivo. J Immunol 2004; 173: 3601-3911.
30. Zampetaki A, Zhang Hu Y, Xu Q. Biomechanical stress induces IL-6 expression in smooth muscle cells via Ras/Rac1-p38 Mapk-NF-kappaB signaling pathways. Am J Physiol Heart Circ Physiol 2005; 288: H2946-H2954.
31. Sanchez C, Gabay O, Salvat C et al. Mechanical loading highly increases IL-6 production and decreases OPG expression by osteoblasts. Osteoarthritis Cartilage 2009; 17: 473-481.
32. Deschner J, Rath-Deschner B, Agarwal S. Regulation of matrix metalloproteinase expression by dynamic tensile strain in rat fibrochondrocytes. Osteoarthritis Cartilage 2006; 14: 264-272.
33. Cummins PM, von Offenberg SN, Killeen MY et al. Cyclic strain-mediated matrix metalloproteinase regulation within the vascular endothelium: a force to be reckoned with PA. Am J Physiol Heart Circ Physiol 2006; 292: H28-H42.
34. Kreidberg JA, Donovan MJ, Goldstein SL et al. Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. Development 1996; 122: 3537-3547.
35. Sachs N, Kreft M, van den Bergh Weerman MA et al. Kidney failure in mice lacking the tetraspanin CD151. J Cell Biol 2006; 175: 33-39.
36. Baleato RM, Guthrie PL, Gubler MC et al. Deletion of CD151 results in a strain-dependent glomerular disease due to severe alterations of the glomerular basement membrane. Am J Pathol 2008; 173: 927-937.
37. Kanasaki K, Kanda Y, Palmsten K et al. Integrin beta1-mediated matrix assembly and signaling are critical for the normal development and function of the kidney glomerulus. Dev Biol 2008; 313: 584-593.
38. Pozzi A, Jarad G, Moeckel GW et al. Beta1 integrin expression by podocytes is required to maintain glomerular structural integrity. Dev Biol 2008; 316: 288-301.
39. Dai C, Stolz DB, Bastacky SI et al. Essential role of integrin-linked kinase in podocyte biology: Bridging the integrin and slit diaphragm signaling. J Am Soc Nephrol 2006; 17: 2164-2175.
40. El-Aouni C, Herbach N, Blattner SM et al. Podocyte-specific deletion of integrin-linked kinase results in severe glomerular basement membrane alterations and progressive glomerulosclerosis. J Am Soc Nephrol 2006; 17: 1334-1344.
41. Kos CH, Le TC, Sinha S et al. Mice deficient in alpha-actinin-4 have severe glomerular disease. J Clin Invest 2003; 111: 1683-1690.
42. Gross O, Beirowski B, Koepke ML et al. Preemptive ramipril therapy delays renal failure and reduces renal fibrosis in COL4A3-knockout mice with Alport syndrome. Kidney Int 2003; 63: 438-446.
43. Shankland SJ, Pippin JW, Reiser J et al. Podocytes in culture: past, present, and future. Kidney Int 2007; 72: 26-36.
44. Rao VH, Lees GE, Kashtan CE et al. Increased expression of MMP-2, MMP-9 (type IV collagenases/gelatinases), and MT1-MMP in canine X-linked Alport syndrome (XLAS). Kidney Int 2003; 63: 1736-1748.
45. Kikkawa Y, Sanzen N, Sekiguchi K. Isolation and characterization of laminin-10/11 secreted by human lung carcinoma cells. laminin-10/11 mediates cell adhesion through integrin alpha3 beta1. J Biol Chem 1998; 273: 15854-15859.
46. Kikkawa Y, Virtanen I, Miner JH. Mesangial cells organize the glomerular capillaries by adhering to the G domain of laminin alpha5 in the glomerular basement membrane. J Cell Biol 2003; 161: 187-196.