Megalin-mediated tubuloglomerular alterations in high-fat diet–induced kidney disease

Journal of the American Society of Nephrology

Volumn 27, Issue 7, 2016, Pages 1996-2008

  Kuwahara, Shoji ^a   Hosojima, Michihiro ^a   Kaneko, Reika ^a   Aoki, Hiroyuki ^a   Nakano, Daisuke ^b   Sasagawa, Taiji ^a   Kabasawa, Hideyuki ^a   Kaseda, Ryohei ^a   Yasukawa, Ryota ^a   Ishikawa, Tomomi ^a   Suzuki, Akiyo ^a,d   Sato, Hiroyoshi ^a   Kageyama, Shun ^a   Tanaka, Takahiro ^c   Kitamura, Nobutaka ^c   Narita, Ichiei ^a   Komatsu, Masaaki ^a   Nishiyama, Akira ^b   Saito, Akihiko ^a  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^b KAGAWA UNIVERSITY   (Japan)

^c NIIGATA UNIVERSITY MEDICAL AND DENTAL HOSPITAL   (Japan)

^d Niigata University   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; CHOLESTEROL; FATTY ACID; GLUCOSE; LIPOFUSCIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MEGALIN; MONOCYTE CHEMOTACTIC PROTEIN 1; ORGANIC ANION TRANSPORTER 1; PLATELET DERIVED GROWTH FACTOR B; SMALL INTERFERING RNA; LRP2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOLYSOSOME; AUTOPHAGY; CELL EXPANSION; CELL VACUOLE; CONTROLLED STUDY; DIET INDUCED OBESITY; DYSLIPIDEMIA; ENDOCYTOSIS; GENE EXPRESSION; GLOMERULUS; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; KIDNEY DISEASE; KIDNEY FIBROSIS; KIDNEY HYPERTROPHY; KIDNEY MASS; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; KNOCKOUT MOUSE; LASER MICROSCOPY; LIPID DIET; LIPID PEROXIDATION; MALE; METABOLIC SYNDROME X; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; TOTAL CHOLESTEROL LEVEL; UPREGULATION; ADVERSE EFFECTS; ANIMAL; CELL CULTURE; COMPARATIVE STUDY; EPITHELIUM CELL; KIDNEY DISEASES; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; DIET, HIGH-FAT; EPITHELIAL CELLS; KIDNEY DISEASES; KIDNEY GLOMERULUS; KIDNEY TUBULES, PROXIMAL; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-2; MALE; MICE; MICE, KNOCKOUT;

EID: 85012039001     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015020190     Document Type: Article

References (47)

1. Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ, Singh GM, Gutierrez HR, Lu Y, Bahalim AN, Farzadfar F, Riley LM, Ezzati M; Global Burden of Metabolic Risk Factors of Chronic Diseases Collaborating Group (Body Mass Index): National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9z1 million participants. Lancet 377: 557–567, 2011
2. Cerezo C, Segura J, Praga M, Ruilope LM: Guidelines updates in the treatment of obesity or metabolic syndrome and hypertension. Curr Hypertens Rep 15: 196–203, 2013
3. Stenvinkel P, Zoccali C, Ikizler TA: Obesity in CKD – what should ne-phrologists know? J Am Soc Nephrol 24: 1727–1736, 2013
4. Kambham N, Markowitz GS, Valeri AM, Lin J, D’Agati VD: Obesity-related glomerulopathy: an emerging epidemic. Kidney Int 59: 1498–1509, 2001
5. Praga M, Hernández E, Morales E, Campos AP, Valero MA, Martínez MA, León M: Clinical features and long-term outcome of obesity-associated focal segmental glomerulosclerosis. Nephrol Dial Transplant 16: 1790–1798, 2001
6. Saito A, Pietromonaco S, Loo AK, Farquhar MG: Complete cloning and sequencing of rat gp330/“megalin,” a distinctive member of the low density lipoprotein receptor gene family. Proc Natl Acad Sci USA 91: 9725–9729, 1994
7. Christensen EI, Nielsen S, Moestrup SK, Borre C, Maunsbach AB, de Heer E, Ronco P, Hammond TG, Verroust P: Segmental distribution of the endocytosis receptor gp330 in renal proximal tubules. Eur J Cell Biol 66: 349–364, 1995
8. Biemesderfer D: Regulated intramembrane proteolysis of megalin: linking urinary protein and gene regulation in proximal tubule? Kidney Int 69: 1717–1721, 2006
9. Shah M, Baterina OY Jr, Taupin V, Farquhar MG: ARH directs megalin to the endocytic recycling compartment to regulate its proteolysis and gene expression. J Cell Biol 202: 113–127, 2013
10. Saito A, Sato H, Iino N, Takeda T: Molecular mechanisms of receptor-mediated endocytosis in the renal proximal tubular epithelium. J Biomed Biotechnol 2010: 403272, 2010
11. Leheste JR, Melsen F, Wellner M, Jansen P, Schlichting U, Renner-Müller I, Andreassen TT, Wolf E, Bachmann S, Nykjaer A, Willnow TE: Hypocalcemia and osteopathy in mice with kidney-specific megalin gene defect. FASEB J 17: 247–249, 2003
12. Weyer K, Storm T, Shan J, Vainio S, Kozyraki R, Verroust PJ, Christensen EI, Nielsen R: Mouse model of proximal tubule endocytic dysfunction. Nephrol Dial Transplant 26: 3446–3451, 2011
13. Kantarci S, Al-Gazali L, Hill RS, Donnai D, Black GC, Bieth E, Chassaing N, Lacombe D, Devriendt K, Teebi A, Loscertales M, Robson C, Liu T, MacLaughlin DT, Noonan KM, Russell MK, Walsh CA, Donahoe PK, Pober BR: Mutations in LRP2, which encodes the multiligand receptor megalin, cause Donnai-Barrow and facio-oculo-acoustico-renal syndromes. Nat Genet 39: 957–959, 2007
14. Weinberg JM: Lipotoxicity. Kidney Int 70: 1560–1566, 2006
15. Thomas MC: Advanced glycation end products. Contrib Nephrol 170: 66–74, 2011
16. Deji N, Kume S, Araki S, Soumura M, Sugimoto T, Isshiki K, Chin-Kanasaki M, Sakaguchi M, Koya D, Haneda M, Kashiwagi A, Uzu T: Structural and functional changes in the kidneys of high-fat diet-induced obese mice. Am J Physiol Renal Physiol 296: F118–F126, 2009
17. Tojo A, Sekine T, Nakajima N, Hosoyamada M, Kanai Y, Kimura K, Endou H: Immunohistochemical localization of multispecific renal organic anion transporter 1 in rat kidney. J Am Soc Nephrol 10: 464–471, 1999
18. Yamahara K, Kume S, Koya D, Tanaka Y, Morita Y, Chin-Kanasaki M, Araki H, Isshiki K, Araki S, Haneda M, Matsusaka T, Kashiwagi A, Maegawa H, Uzu T: Obesity-mediated autophagy insufficiency exacerbates proteinuria-induced tubulointerstitial lesions. J Am Soc Nephrol 24: 1769–1781, 2013
19. Cao X, Xue L, Han L, Ma L, Chen T, Tong T: WW domain-containing E3 ubiquitin protein ligase 1 (WWP1) delays cellular senescence by promoting p27(Kip1) degradation in human diploid fibroblasts. J Biol Chem 286: 33447–33456, 2011
20. Gahan PB: Histochemistry of lysosomes. Int Rev Cytol 21: 1–63, 1967
21. Declèves AE, Zolkipli Z, Satriano J, Wang L, Nakayama T, Rogac M, Le TP, Nortier JL, Farquhar MG, Naviaux RK, Sharma K: Regulation of lipid accumulation by AMP-activated kinase [corrected] in high fat diet-induced kidney injury. Kidney Int 85: 611–623, 2014
22. Panossian L, Fenik P, Zhu Y, Zhan G, McBurney MW, Veasey S: SIRT1 regulation of wakefulness and senescence-like phenotype in wake neurons. J Neurosci 31: 4025–4036, 2011
23. Schönenbrücher H, Adhikary R, Mukherjee P, Casey TA, Rasmussen MA, Maistrovich FD, Hamir AN, Kehrli ME Jr, Richt JA, Petrich JW: Fluorescence-based method, exploiting lipofuscin, for real-time detection of central nervous system tissues on bovine carcasses. J Agric Food Chem 56: 6220–6226, 2008
24. Negre-Salvayre A, Auge N, Ayala V, Basaga H, Boada J, Brenke R, Chapple S, Cohen G, Feher J, Grune T, Lengyel G, Mann GE, Pamplona R, Poli G, Portero-Otin M, Riahi Y, Salvayre R, Sasson S, Serrano J, Shamni O, Siems W, Siow RC, Wiswedel I, Zarkovic K, Zarkovic N: Pathological aspects of lipid peroxidation. Free Radic Res 44: 1125–1171, 2010
25. Itakura K, Oya-Ito T, Osawa T, Yamada S, Toyokuni S, Shibata N, Kobayashi M, Uchida K: Detection of lipofuscin-like fluorophore in oxidized human low-density lipoprotein. 4-hydroxy-2-nonenal as a potential source of fluorescent chromophore. FEBS Lett 473: 249–253, 2000
26. Kerjaschki D, Exner M, Ullrich R, Susani M, Curtiss LK, Witztum JL, Farquhar MG, Orlando RA: Pathogenic antibodies inhibit the binding of apolipoproteins to megalin/gp330 in passive Heymann nephritis. J Clin Invest 100: 2303–2309, 1997
27. Hall AM, Rhodes GJ, Sandoval RM, Corridon PR, Molitoris BA: In vivo multiphoton imaging of mitochondrial structure and function during acute kidney injury. Kidney Int 83: 72–83, 2013
28. Nishioka S, Nakano D, Kitada K, Sofue T, Ohsaki H, Moriwaki K, Hara T, Ohmori K, Kohno M, Nishiyama A: The cyclin-dependent kinase inhibitor p21 is essential for the beneficial effects of renal ischemic preconditioning on renal ischemia/reperfusion injury in mice. Kidney Int 85: 871–879, 2014
29. Schrimpf C, Duffield JS: Mechanisms of fibrosis: the role of the pericyte. Curr Opin Nephrol Hypertens 20: 297–305, 2011
30. Lin SL, Chang FC, Schrimpf C, Chen YT, Wu CF, Wu VC, Chiang WC, Kuhnert F, Kuo CJ, Chen YM, Wu KD, Tsai TJ, Duffield JS: Targeting endothelium-pericyte cross talk by inhibiting VEGF receptor signaling attenuates kidney microvascular rarefaction and fibrosis. Am J Pathol 178: 911–923, 2011
31. Chen YT, Chang FC, Wu CF, Chou YH, Hsu HL, Chiang WC, Shen J, Chen YM, Wu KD, Tsai TJ, Duffield JS, Lin SL: Platelet-derived growth factor receptor signaling activates pericyte-myofibroblast transition in obstructive and post-ischemic kidney fibrosis. Kidney Int 80: 1170–1181, 2011
32. Fredriksson L, Li H, Eriksson U: The PDGF family: four gene products form five dimeric isoforms. Cytokine Growth Factor Rev 15: 197–204, 2004
33. Tang WW, Ulich TR, Lacey DL, Hill DC, Qi M, Kaufman SA, Van GY, Tarpley JE, Yee JS: Platelet-derived growth factor-BB induces renal tubulointerstitial myofibroblast formation and tubulointerstitial fibrosis. Am J Pathol 148: 1169–1180, 1996
34. Motoyoshi Y, Matsusaka T, Saito A, Pastan I, Willnow TE, Mizutani S, Ichikawa I: Megalin contributes to the early injury of proximal tubule cells during nonselective proteinuria. Kidney Int 74: 1262–1269, 2008
35. Theilig F, Kriz W, Jerichow T, Schrade P, Hähnel B, Willnow T, Le Hir M, Bachmann S: Abrogation of protein uptake through megalin-deficient proximal tubules does not safeguard against tubulointerstitial injury. J Am Soc Nephrol 18: 1824–1834, 2007
36. Jiang M, Liu K, Luo J, Dong Z: Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury. Am J Pathol 176: 1181–1192, 2010
37. Kimura T, Takabatake Y, Takahashi A, Kaimori JY, Matsui I, Namba T, Kitamura H, Niimura F, Matsusaka T, Soga T, Rakugi H, Isaka Y: Autophagy protects the proximal tubule from degeneration and acute ischemic injury. J Am Soc Nephrol 22: 902–913, 2011
38. Jiang M, Wei Q, Dong G, Komatsu M, Su Y, Dong Z: Autophagy in proximal tubules protects against acute kidney injury. Kidney Int 82: 1271–1283, 2012
39. Liu D, Wen Y, Tang TT, Lv LL, Tang RN, Liu H, Ma KL, Crowley SD, Liu BC: Megalin/cubulin-lysosome-mediated albumin reabsorption is involved in the tubular cell activation of NLRP3 inflammasome and tubulointerstitial inflammation. J Biol Chem 290: 18018–18028, 2015
40. Madsen KM, Park CH: Lysosome distribution and cathepsin B and L activity along the rabbit proximal tubule. Am J Physiol 253: F1290–F1301, 1987
41. Ivy GO, Roopsingh R, Kanai S, Ohta M, Sato Y, Kitani K: Leupeptin causes an accumulation of lipofuscin-like substances and other signs of aging in kidneys of young rats: further evidence for the protease inhibitor model of aging. Ann N Y Acad Sci 786: 12–23, 1996
42. Reisman SA, Chertow GM, Hebbar S, Vaziri ND, Ward KW, Meyer CJ: Bardoxolone methyl decreases megalin and activates nrf2 in the kidney. J Am Soc Nephrol 23: 1663–1673, 2012
43. Pergola PE, Raskin P, Toto RD, Meyer CJ, Huff JW, Grossman EB, Krauth M, Ruiz S, Audhya P, Christ-Schmidt H, Wittes J, Warnock DG; BEAM Study Investigators: Bardoxolone methyl and kidney function in CKD with type 2 diabetes. N Engl J Med 365: 327–336, 2011
44. Tsuboi N, Utsunomiya Y, Kanzaki G, Koike K, Ikegami M, Kawamura T, Hosoya T: Low glomerular density with glomerulomegaly in obesity-related glomerulopathy. Clin J Am Soc Nephrol 7: 735–741, 2012
45. Hosaka K, Takeda T, Iino N, Hosojima M, Sato H, Kaseda R, Yamamoto K, Kobayashi A, Gejyo F, Saito A: Megalin and nonmuscle myosin heavy chain IIA interact with the adaptor protein Disabled-2 in proximal tubule cells. Kidney Int 75: 1308–1315, 2009
46. Nakano D, Doi K, Kitamura H, Kuwabara T, Mori K, Mukoyama M, Nishiyama: A reduction of tubular flow rate as a mechanism of oliguria in the early phase of endotoxemia revealed by intravital imaging [published online ahead of print April 8, 2015]. J Am Soc Nephrol doi: 10.1681/ASN.2014060577
47. Bampton ET, Goemans CG, Niranjan D, Mizushima N, Tolkovsky AM: The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lysosomes. Autophagy 1: 23–36, 2005