The renoprotective effects of soy protein in the aging kidney
Main Article Content
Abstract
Aging is a risk factor for chronic kidney disease (CKD) and is itself associated with alterations in renal structure and function. There are no specific interventions to attenuate age-dependent renal dysfunction and the mechanism(s) responsible for these deficits have not been fully elucidated. In this study, male Fischer 344 rats, which develop age-dependent nephropathy, were feed a casein- or soy protein diet beginning at 16 mon (late life intervention) and renal structure and function was assessed at 20 mon. The soy diet did not significantly affect body weight, but was renoprotective as assessed by decreased proteinuria, increased glomerular filtration rate (GFR) and decreased urinary kidney injury molecule-1 (Kim-1). Renal fibrosis, as assessed by hydroxyproline content, was decreased by the soy diet, as were several indicators of inflammation. RNA sequencing identified several candidates for the renoprotective effects of soy, including decreased expression of Twist2, a basic helix-loop-helix transcription factor that network analysis suggest may regulate the expression of several genes associated with renal dysfunction. Twist2 expression is upregulated in the aging kidney and the unilateral ureteral obstruction of fibrosis; the expression is limited to distal tubules of mice. Taken together, these data demonstrate the renoprotective potential of soy protein, putatively by reducing inflammation and fibrosis, and identify Twist2 as a novel mediator of renal dysfunction that is targeted by soy.
Keywords:
aging, chronic kidney disease, fibrosis, inflammation, soy, Twist2
Article Details
How to Cite
GRUNZ-BORGMANN, Elizabeth A. et al.
The renoprotective effects of soy protein in the aging kidney.
Medical Research Archives, [S.l.], v. 8, n. 3, mar. 2020.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2065>. Date accessed: 22 dec. 2024.
doi: https://doi.org/10.18103/mra.v8i3.2065.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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15. Palanisamy N, Venkataraman Anuradha C. Soy protein prevents renal damage in a fructose-induced model of metabolic syndrome via inhibition of NF-kB in male rats. Pediatr Nephrol. 2011 Oct; 26(10):1809-1821.
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22. Nichols LA, Grunz-Borgmann EA, Wang X, Parrish AR. A role for the age-dependent loss of a(E)-catenin in regulation of N-cadherin expression and cell migration. Physiol Rep. 2014 Jun 11: 2(6):e12039.
23. Slusarz A, Nichols LA, Grunz-Borgmann EA, Chen G, Akintola AD, Catania JM, Burghardt RC, Trzeciakowski JP, Parrish AR. Overexpression of MMP-7 increases collagen 1A2 in the aging kidney. Physiol Rep. 2013 Oct: 1(5):e00090.
24. Wang X, Grunz-Borgmann EA, Parrish AR. Loss of a(E)-catenin potentiates cisplatin-induced nephrotoxicity via increasing apoptosis in renal tubular epithelial cells. Toxicol Sci. 2014 Sep; 141(1):254-262.
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26. Bonventre JV. Kidney injury molecule-1 (Kim-1): A specific and sensitive biomarker of kidney injury. Scand J Clin Lab Invest Suppl. 2008; 241:78-83.
27. Chen G, Bridenbaugh EA, Akintola AD, Catania JM, Vaidya VS, Bonventre JV, Dearman AC, Sampson HW, Zawieja DC, Burghardt RC, Parrish AR. Increased susceptibility of aging kidney to ischemic injury: Identification of candidate genes changed during aging, but corrected by caloric restriction. Am J Physiol Renal Physiol. 2007 Oct; 293(4):F1272-F1281.
28. Gardiner L, Akintola A, Chen G, Catania JM, Vaidya V, Burghardt RC, Bonventre JV, Trzeciakowski J, Parrish AR. Structural equation modeling highlights the potential of Kim-1 as a biomarker for chronic kidney disease. Am J Nephrol. 2012; 35(2):152-163.
29. Humphreys BD, Xu F, Sabbisetti V, Grgic I, Movahedi Naini S, Wang N, Chen G, Xiao S, Patel D, Henderson JM, Ichimura T, Mou S, Soeung S, McMahon AP, Kuchroo VK, Bonventre JV. Chronic epithelial kidney injury molecule-1 expression causes murine kidney fibrosis J Clin Invest. 2013 Sep; 123(9):4023-4035.
30. Horio M, Imai E, Yasuda Y, Watanabe T, Matsuo S; Collaborators Developing the Japanese Equation for Estimated GFR. GFR estimation using standardized serum cystatin C in Japan. Am J Kidney Dis. 2013 Feb; 61(2):197-203.
31. Qiao X, Li RS, Li H, Zhu GZ, Huang XG, Shao S, Bai B. Intermedin protects against renal ischemia-reperfusion by inhibition of oxidative stress. Am J Physiol Renal Physiol. 2013 Jan; 304(1):F112-F119.
32. Franco HL, Casasnovas J, Rodriguez-Medina JR, Cadilla CL. Redundant or separate entities? – roles of Twist1 and Twist2 as molecular switches during gene transcription. Nucleic Acid Res. 2011 Mar; 39(4):1177-1186.
33. Zeisberg M, Neilson EG. Mechanisms of tubulointerstitial fibrosis. J Am Soc Nephrol. 2010 Nov; 21(11):1819-1834.
34. Yang HY, Chen JR. Renoprotective effects of soy protein hydrolysates in N(omega)-nitro-L-arginine methyl ester hydrochloride induced hypertensive rats. Hypertens Res. 2008 Jul; 31(7):1477-1483.
35. Velasquez MT, Bhathena SJ. Dietary phytoestrogens: A possible role in renal disease protection. Am J Kidney Dis. 2001 May; 37(5):1056-1068.
36. Fanti P, Asmis R, Stephenson TJ, Sawaya BP, Franke AA. Positive effect of dietary soy in ESRD patients with systemic inflammation--correlation between blood levels of the soy isoflavones and the acute-phase reactants. Nephrol Dial Transplant. 2006 Aug: 21(8):2239-2246.
37. Vielhauer V, Berning E, Eis V, Kretzler M, Segerer S, Strutz F, Horuk R, Grone HJ, Schlondorff D, Anders HJ. CCR1 blockade reduces interstitial fibrosis in mice with glomerulosclerosis and nephrotic syndrome. Kidney Int. 2004 Dec; 66(6):2264-2278.
38. Murakami M, Ohkuma M, Nakamura M. Molecular mechanism of transforming growth factor-beta-mediated inhibition of growth arrest and differentiation in a myoblast cell line. Dev Growth Differ. 2008 Feb; 50(2):121-130.
39. Marchegiani S, Davis T, Tessadori, van Haaften G, Brancati F, Hoischen A, Huang H, Valkanas E, Pusey B, Schanze D, Venselaar H, Vulto-van Silfhout AT, Wolfe LA, Tifft CJ, Zerfas PM, Zambruno G, Kariminejad A, Sabbagh-Kermani F, Lee J, Tsokos MG, Lee CC, Ferraz V, da Silva EM, Stevens CA, Roche N, Bartsch O, Farndon P, Bermejo-Sanchez E, Brooks BP, Maduro V, Dallapiccola B, Ramos FJ, Chung HY, Le Caignec C, Martins F, Jacyk WK, Mazzanti L, Brunner HG, Bakkers J, Lin S, Malicdan MC, Boerkoel CF, Gahl WA, da Vries BB, van Haelst MM, Zenker M, Markello TC. Recurrent mutations in the basic domain of Twist2 cause ablepharon macrostomia and Barber-Say syndrome. Am J Hum Genet. 2015 Jul 2; 97(1):99-110.
40. Rosti RO, Uyguner ZO, Nazarenko I, Bekerecioglu M, Cadilla CL, Ozgur H, Lee BH, Aggarwal AK, Pehlivan S, Desnick RJ. Setleis syndrome: Clinical, molecular and structural studies of the first Twist2 missense mutation. Clin Genet. 2015 Nov; 88(5):489-493.
41. Girisha KM, Bidchol AM, Sarpangala MK, Satyamoorthy K. A novel frameshift in Twist2 causing Setleis syndrome. Indian J Pediatr. 2014 Mar; 81(3):302-304.
42. Grunz-Borgmann EA, Nichols LA, Wang X, Parrish AR. Twist2 is upregulated in early stages of repair following acute kidney injury. Int J Mol Sci. 2017 Feb 10; 18(2):E368.
43. Ogborn MR, Nitschmann E, Bankovic-Calic N, Weiler HA, Aukema HM. Dietary soy protein benefit in experimental kidney disease is preserved after isoflavone depletion of diet. Expt Biol Med. 2010 Nov; 235(11):1315-1320.
44. Davis J, Higginbotham A, O’Connor T, Moustaid-Moussa N, Tebbe A, Kim YC, Cho KW, Shay N, Adler S, Peterson R, Banz W. Soy protein and isoflavones influence adiposity and development of metabolic syndrome in the obsese male ZDF rat. Ann Nutr Metab. 2007; 51(1):42-52.
45. de Mejia EG, Dia VP. Lunasin and lunasin-like peptides inhibit inflammation through suppression of NF-kappaB pathway in macrophage. Peptides. 2009 Dec; 30912):2388-2398.
46. Bialek P, Kern B, Yang X, Schrock M, Sosic D, Hong N, Wu H, Yu K, Ornitz DM, Olson EN, Justice MJ, Karsenty G. A twist code determines the onset of osteoblast differentiation. Dev Cell. 2004 Mar; 6(3):423-435.
47. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinbeg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004 Jun 25; 117(7):927-939.
48. Kida Y, Asahina K, Teraoka H, Gitelman I, Sato T. Twist relates to tubular epithelial-mesenchymal transition and interstitial fibrogenesis in the obstructed kidney. J Histochem Cytochem. 2007 Jul; 55(7):661-673.
49. Lovisa S, LeBleu VS, Tampe B, Sugimoto H, Vadnagara K, Carstens JL, Wu CC, Hagos Y, Burckhardt BC, Pentcheva-Hoang T, Nischal H, Allison JP, Zeisberg M, Kalluri R. Epithelial-to-mesenchymal transition induces cell cycle arrest and parenchymal damage in renal fibrosis. Nat Med. 2015 Sep; 21(9):998-1009.
50. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012 Mar 4; 9(4):357-359.
51. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012 Mar 1; 7(3):562-578.
52. Zhu M, Dahmen JL, Stacey G, Cheng J. Predicting gene regulatory networks of soybean nodulation from RNA-Seq transcriptome data. BMC Bioinformatics. 2013 Sep 22; 14:278.
53. Zhu M, Deng X, Joshi T, Xu D, Stacey G, Cheng J. Reconstructing differentially co-expressed gene modules and regulatory networks of soybean cells. BMC Genomics. 2012 Aug 31; 13:437.
Li J, Hou J, Sun L, Wilkins JM, Lu Y, Niederhuth CE, Merideth BR, Mawhinney TP, Mossine VV, Greenlief CM, Walker JC, Folk WR, Hannink M, Lubahn DB, Birchier JA, Cheng J. From gigabyte to kilobyte: a bioinformatics protocol for mining large RNA-Seq transcriptomics data. PloS One. 2015 Apr 22; 10(4):e0125000
2. Zhang QL, Rothenbacher D. Prevalence of chronic kidney disease in population-based studies: Systemic review. BMC Public Health. 2008 Apr 11; 8:117.
3. Jassal SV, Oreopoulos DG. The aging kidney. Geriatric Nephrol Urol. 1998 8(3):141-147.
4. Lindeman RD, Tobin J, Shock NW. Longitudinal studies on the rate of decline in renal function with age. J Am Geriatr Soc. 1985 April; 33(4):278-285, 1985.
5. Musso CG, Macias Nunez JF, Oreopoulos DG. Physiological similarities and differences between renal aging and chronic renal disease. J Nephrol. 2007 Sep-Oct; 20(5):586-587.
6. Coresh J, Selvin E, Stevens LA, Manzi J, Kusek JW, Eggers P, Van Lente F, Levey AS. Prevalence of chronic kidney disease in the United States. J Am Med Assoc. 2007 Nov 7; 298(17):2038-2047.
7. Haley DP, Bulger RE. The aging male rat: Structure and function of the kidney. Am J Anat. 1983 May; 167(1):1-13.
8. Sands JM. Urine-concentrating ability in the aging kidney. Sci Aging Knowledge Environ. 2003 Jun 18; 2003(24):PE15.
9. Corman B, Owen R. Normal development, growth, and aging of the kidney, in Pathobiology of Aging Rats, Mohr U, Dungworth DL, Capen CC, Washington DC (eds). ILSI Press, pp 195-209, 1992.
10. Kalu DN, Masoro EJ, Yu BP, Hardin RR, Hollis BW. Modulation of age-related hyperparathyroidism and senile bone loss in Fischer rats by soy protein and food restriction. Endocrinology. 1988 May; 122(5):1847-1854.
11. Iwasaki K, Gleiser CA, Masoro EJ, McMahan CA, Seo EJ, Yu BP. The influence of dietary protein source on longevity and age-related disease processes of Fischer rats. J Gerontol. 1988 Jan; 43(1):B5-12.
12. Aukema HM, Housini I, Rawling JM. Dietary soy protein effects on inherited polycystic kidney disease are influenced by gender and protein level. J Am Soc Nephrol. 1999 Feb; 10(2):300-308.
13. Tomobe K, Philbrick DJ, Ogborn MR, Takahashi H, Holub BJ. Effect of dietary soy protein and genistein on disease progression in mice with polycystic kidney disease. Am J Kidney Dis. 1998 Jan; 31(1):55-61.
14. Philbrick DJ, Bureau DP, Colins FW, Holub BJ. Evidence that soyasaponin Bb retards disease progression in a murine model of polycystic kidney disease. Kidney Int. 2003 Apr; 63(4):1230-1239.
15. Palanisamy N, Venkataraman Anuradha C. Soy protein prevents renal damage in a fructose-induced model of metabolic syndrome via inhibition of NF-kB in male rats. Pediatr Nephrol. 2011 Oct; 26(10):1809-1821.
16. Palanisamy N, Kannapan S, Anuradha CV. Genistein modulates NF-kB-associated renal inflammation, fibrosis and podocyte abnormalities in fructose-fed rats. Eur J Pharmacol. 2011 Sep 30; 667(1-3):355-364.
17. Davis J, Iqbal MJ, Steinle J, Oitker J, Higginbotham DA, Peterson RG, Banz WJ. Soy protein influences the development of the metabolic syndrome in male obese ZDFxSHHF rats. Horm Metab Res. 2005 Natl 37(5):316-325.
18. Azadbakht L, Shakerhosseini R, Atabak S, Jamshidian M, Mehrabi Y, Esmaill-Zadeh A. Beneficiary effect of dietary soy protein on lowering plasma levels of lipid and improving kidney function in type II diabetes with nephropathy. Eur J Clin Nutr. 2003 Oct; 57(10):1292-1294.
19. Azadbakht L, Atabak S, Esmaillzadeh A. Soy protein intake, cardiorenal indices, and C-reactive protein in type 2 diabetes with nephropathy: A longitudinal randomized clinical trial. Diabetes Care. 2008 Apr; 31(4):648-654.
20. Teixeira SR, Tappenden KA, Carson L, Jones R, Prabhudesai M, Marshall WP, Erdman JW Jr. Isolated soy protein consumption reduces urinary albumin excretion and improves the serum lipid profile in men with type 2 diabetes mellitus and nephropathy. J Nutr. 2004 Aug; 134(8):1874-1880.
21. Akintola AD, Crislip ZL, Catania JM, Chen G, Zimmer WE, Burghardt RC, Parrish AR. Promoter methylation is associated with the age-dependent loss of N-cadherin in the rat kidney. Am J Physiol: Renal Physiol. 2008 Jan; 294(1):F170-F176.
22. Nichols LA, Grunz-Borgmann EA, Wang X, Parrish AR. A role for the age-dependent loss of a(E)-catenin in regulation of N-cadherin expression and cell migration. Physiol Rep. 2014 Jun 11: 2(6):e12039.
23. Slusarz A, Nichols LA, Grunz-Borgmann EA, Chen G, Akintola AD, Catania JM, Burghardt RC, Trzeciakowski JP, Parrish AR. Overexpression of MMP-7 increases collagen 1A2 in the aging kidney. Physiol Rep. 2013 Oct: 1(5):e00090.
24. Wang X, Grunz-Borgmann EA, Parrish AR. Loss of a(E)-catenin potentiates cisplatin-induced nephrotoxicity via increasing apoptosis in renal tubular epithelial cells. Toxicol Sci. 2014 Sep; 141(1):254-262.
25. Grunz-Borgmann EA, Nichols LA, Wiedmeyer CE, Spagnoli S, Trzeciakowski JP, Parrish AR. Structural equation modeling identifies markers of damage and function in the aging male Fischer 344 rat. Mech Ageing Dev. 2016 Jun; 156:55-62.
26. Bonventre JV. Kidney injury molecule-1 (Kim-1): A specific and sensitive biomarker of kidney injury. Scand J Clin Lab Invest Suppl. 2008; 241:78-83.
27. Chen G, Bridenbaugh EA, Akintola AD, Catania JM, Vaidya VS, Bonventre JV, Dearman AC, Sampson HW, Zawieja DC, Burghardt RC, Parrish AR. Increased susceptibility of aging kidney to ischemic injury: Identification of candidate genes changed during aging, but corrected by caloric restriction. Am J Physiol Renal Physiol. 2007 Oct; 293(4):F1272-F1281.
28. Gardiner L, Akintola A, Chen G, Catania JM, Vaidya V, Burghardt RC, Bonventre JV, Trzeciakowski J, Parrish AR. Structural equation modeling highlights the potential of Kim-1 as a biomarker for chronic kidney disease. Am J Nephrol. 2012; 35(2):152-163.
29. Humphreys BD, Xu F, Sabbisetti V, Grgic I, Movahedi Naini S, Wang N, Chen G, Xiao S, Patel D, Henderson JM, Ichimura T, Mou S, Soeung S, McMahon AP, Kuchroo VK, Bonventre JV. Chronic epithelial kidney injury molecule-1 expression causes murine kidney fibrosis J Clin Invest. 2013 Sep; 123(9):4023-4035.
30. Horio M, Imai E, Yasuda Y, Watanabe T, Matsuo S; Collaborators Developing the Japanese Equation for Estimated GFR. GFR estimation using standardized serum cystatin C in Japan. Am J Kidney Dis. 2013 Feb; 61(2):197-203.
31. Qiao X, Li RS, Li H, Zhu GZ, Huang XG, Shao S, Bai B. Intermedin protects against renal ischemia-reperfusion by inhibition of oxidative stress. Am J Physiol Renal Physiol. 2013 Jan; 304(1):F112-F119.
32. Franco HL, Casasnovas J, Rodriguez-Medina JR, Cadilla CL. Redundant or separate entities? – roles of Twist1 and Twist2 as molecular switches during gene transcription. Nucleic Acid Res. 2011 Mar; 39(4):1177-1186.
33. Zeisberg M, Neilson EG. Mechanisms of tubulointerstitial fibrosis. J Am Soc Nephrol. 2010 Nov; 21(11):1819-1834.
34. Yang HY, Chen JR. Renoprotective effects of soy protein hydrolysates in N(omega)-nitro-L-arginine methyl ester hydrochloride induced hypertensive rats. Hypertens Res. 2008 Jul; 31(7):1477-1483.
35. Velasquez MT, Bhathena SJ. Dietary phytoestrogens: A possible role in renal disease protection. Am J Kidney Dis. 2001 May; 37(5):1056-1068.
36. Fanti P, Asmis R, Stephenson TJ, Sawaya BP, Franke AA. Positive effect of dietary soy in ESRD patients with systemic inflammation--correlation between blood levels of the soy isoflavones and the acute-phase reactants. Nephrol Dial Transplant. 2006 Aug: 21(8):2239-2246.
37. Vielhauer V, Berning E, Eis V, Kretzler M, Segerer S, Strutz F, Horuk R, Grone HJ, Schlondorff D, Anders HJ. CCR1 blockade reduces interstitial fibrosis in mice with glomerulosclerosis and nephrotic syndrome. Kidney Int. 2004 Dec; 66(6):2264-2278.
38. Murakami M, Ohkuma M, Nakamura M. Molecular mechanism of transforming growth factor-beta-mediated inhibition of growth arrest and differentiation in a myoblast cell line. Dev Growth Differ. 2008 Feb; 50(2):121-130.
39. Marchegiani S, Davis T, Tessadori, van Haaften G, Brancati F, Hoischen A, Huang H, Valkanas E, Pusey B, Schanze D, Venselaar H, Vulto-van Silfhout AT, Wolfe LA, Tifft CJ, Zerfas PM, Zambruno G, Kariminejad A, Sabbagh-Kermani F, Lee J, Tsokos MG, Lee CC, Ferraz V, da Silva EM, Stevens CA, Roche N, Bartsch O, Farndon P, Bermejo-Sanchez E, Brooks BP, Maduro V, Dallapiccola B, Ramos FJ, Chung HY, Le Caignec C, Martins F, Jacyk WK, Mazzanti L, Brunner HG, Bakkers J, Lin S, Malicdan MC, Boerkoel CF, Gahl WA, da Vries BB, van Haelst MM, Zenker M, Markello TC. Recurrent mutations in the basic domain of Twist2 cause ablepharon macrostomia and Barber-Say syndrome. Am J Hum Genet. 2015 Jul 2; 97(1):99-110.
40. Rosti RO, Uyguner ZO, Nazarenko I, Bekerecioglu M, Cadilla CL, Ozgur H, Lee BH, Aggarwal AK, Pehlivan S, Desnick RJ. Setleis syndrome: Clinical, molecular and structural studies of the first Twist2 missense mutation. Clin Genet. 2015 Nov; 88(5):489-493.
41. Girisha KM, Bidchol AM, Sarpangala MK, Satyamoorthy K. A novel frameshift in Twist2 causing Setleis syndrome. Indian J Pediatr. 2014 Mar; 81(3):302-304.
42. Grunz-Borgmann EA, Nichols LA, Wang X, Parrish AR. Twist2 is upregulated in early stages of repair following acute kidney injury. Int J Mol Sci. 2017 Feb 10; 18(2):E368.
43. Ogborn MR, Nitschmann E, Bankovic-Calic N, Weiler HA, Aukema HM. Dietary soy protein benefit in experimental kidney disease is preserved after isoflavone depletion of diet. Expt Biol Med. 2010 Nov; 235(11):1315-1320.
44. Davis J, Higginbotham A, O’Connor T, Moustaid-Moussa N, Tebbe A, Kim YC, Cho KW, Shay N, Adler S, Peterson R, Banz W. Soy protein and isoflavones influence adiposity and development of metabolic syndrome in the obsese male ZDF rat. Ann Nutr Metab. 2007; 51(1):42-52.
45. de Mejia EG, Dia VP. Lunasin and lunasin-like peptides inhibit inflammation through suppression of NF-kappaB pathway in macrophage. Peptides. 2009 Dec; 30912):2388-2398.
46. Bialek P, Kern B, Yang X, Schrock M, Sosic D, Hong N, Wu H, Yu K, Ornitz DM, Olson EN, Justice MJ, Karsenty G. A twist code determines the onset of osteoblast differentiation. Dev Cell. 2004 Mar; 6(3):423-435.
47. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinbeg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004 Jun 25; 117(7):927-939.
48. Kida Y, Asahina K, Teraoka H, Gitelman I, Sato T. Twist relates to tubular epithelial-mesenchymal transition and interstitial fibrogenesis in the obstructed kidney. J Histochem Cytochem. 2007 Jul; 55(7):661-673.
49. Lovisa S, LeBleu VS, Tampe B, Sugimoto H, Vadnagara K, Carstens JL, Wu CC, Hagos Y, Burckhardt BC, Pentcheva-Hoang T, Nischal H, Allison JP, Zeisberg M, Kalluri R. Epithelial-to-mesenchymal transition induces cell cycle arrest and parenchymal damage in renal fibrosis. Nat Med. 2015 Sep; 21(9):998-1009.
50. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012 Mar 4; 9(4):357-359.
51. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012 Mar 1; 7(3):562-578.
52. Zhu M, Dahmen JL, Stacey G, Cheng J. Predicting gene regulatory networks of soybean nodulation from RNA-Seq transcriptome data. BMC Bioinformatics. 2013 Sep 22; 14:278.
53. Zhu M, Deng X, Joshi T, Xu D, Stacey G, Cheng J. Reconstructing differentially co-expressed gene modules and regulatory networks of soybean cells. BMC Genomics. 2012 Aug 31; 13:437.
Li J, Hou J, Sun L, Wilkins JM, Lu Y, Niederhuth CE, Merideth BR, Mawhinney TP, Mossine VV, Greenlief CM, Walker JC, Folk WR, Hannink M, Lubahn DB, Birchier JA, Cheng J. From gigabyte to kilobyte: a bioinformatics protocol for mining large RNA-Seq transcriptomics data. PloS One. 2015 Apr 22; 10(4):e0125000