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Transcriptomics: a Solution for Renal Osteodystrophy?

  • Kidney and Bone (IB Salusky and T Nickolas, Section Editors)
  • Published:
Current Osteoporosis Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

The molecular mechanisms of the bone disease associated with chronic kidney disease (CKD), called renal osteodystrophy (ROD), are poorly understood. New transcriptomics technologies may provide clinically relevant insights into the pathogenesis of ROD. This review summarizes current progress and limitations in the study and treatment of ROD, and in transcriptomics analyses of skeletal tissues.

Recent Findings

ROD is characterized by poor bone quality and strength leading to increased risk of fracture. Recent studies indicate permanent alterations in bone cell populations during ROD. Single-cell transcriptomics analyses, successful at identifying specialized cell subpopulations in bone, have not yet been performed in ROD.

Summary

ROD is a widespread poorly understood bone disease with limited treatment options. Transcriptomics analyses of bone are needed to identify the bone cell subtypes and their role in the pathogenesis of ROD, and to develop adequate diagnosis and treatment strategies.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. •• Dussold C, Gerber C, White S, Wang X, Qi L, Francis C, et al. DMP1 prevents osteocyte alterations, FGF23 elevation and left ventricular hypertrophy in mice with chronic kidney disease. Bone Research. 2019;7:12 This study shows that osteocyte secretion of DMP1 is reduced in the bone of mice with CKD and that DMP1 repletion reverses ROD.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  2. Pereira RC, Delany AM, Khouzam NM, Bowen RE, Freymiller EG, Salusky IB, et al. Primary osteoblast-like cells from patients with end-stage kidney disease reflect gene expression, proliferation, and mineralization characteristics ex vivo. Kidney Int. 2015;87(3):593–601.

    Article  CAS  PubMed  Google Scholar 

  3. •• Pereira RC, Salusky IB, Roschger P, Klaushofer K, Yadin O, Freymiller EG, et al. Impaired osteocyte maturation in the pathogenesis of renal osteodystrophy. Kidney Int. 2018;94(5):1002–12 This study shows that osteoblast and osteocyte maturation is altered in cell cultures isolated from bone biopsies of pediatric patients with ROD, suggesting that molecular changes affecting bone cells are independent of systemic perturbations.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Chen NX, O'Neill KD, Allen MR, Newman CL, Moe SM. Low bone turnover in chronic kidney disease is associated with decreased VEGF-A expression and osteoblast differentiation. Am J Nephrol. 2015;41(6):464–73.

    Article  CAS  PubMed  Google Scholar 

  5. Coresh J, Selvin E, Stevens LA, Manzi J, Kusek JW, Eggers P, et al. Prevalence of chronic kidney disease in the United States. JAMA. 2007;298(17):2038–47.

    Article  CAS  PubMed  Google Scholar 

  6. Bikbov B, Perico N, Remuzzi G. On behalf of the GBDGDEG. Disparities in chronic kidney disease prevalence among males and females in 195 countries: analysis of the global burden of disease 2016 study. Nephron. 2018;139(4):313–8.

    Article  PubMed  Google Scholar 

  7. Spasovski GB, Bervoets AR, Behets GJ, Ivanovski N, Sikole A, Dams G, et al. Spectrum of renal bone disease in end-stage renal failure patients not yet on dialysis. Nephrol Dial Transplant. 2003;18(6):1159–66.

    Article  CAS  PubMed  Google Scholar 

  8. Hamdy NA, Kanis JA, Beneton MN, Brown CB, Juttmann JR, Jordans JG, et al. Effect of alfacalcidol on natural course of renal bone disease in mild to moderate renal failure. BMJ. 1995;310(6976):358–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Coen G, Mazzaferro S, Bonucci E, Taggi F, Ballanti P, Bianchi AR, et al. Bone GLA protein in predialysis chronic renal failure. Effects of 1,25(OH)2D3 administration in a long-term follow-up. Kidney Int. 1985;28(5):783–90.

    Article  CAS  PubMed  Google Scholar 

  10. Malluche HH, Mawad HW, Monier-Faugere MC. Renal osteodystrophy in the first decade of the new millennium: analysis of 630 bone biopsies in black and white patients. J Bone Miner Res. 2011;26(6):1368–76.

    Article  PubMed  Google Scholar 

  11. Behets GJ, Spasovski G, Sterling LR, Goodman WG, Spiegel DM, De Broe ME, et al. Bone histomorphometry before and after long-term treatment with cinacalcet in dialysis patients with secondary hyperparathyroidism. Kidney Int. 2015;87(4):846–56.

    Article  CAS  PubMed  Google Scholar 

  12. Nickolas TL, Stein EM, Dworakowski E, Nishiyama KK, Komandah-Kosseh M, Zhang CA, et al. Rapid cortical bone loss in patients with chronic kidney disease. J Bone Miner Res. 2013;28(8):1811–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Nickolas TL, McMahon DJ, Shane E. Relationship between moderate to severe kidney disease and hip fracture in the United States. J Am Soc Nephrol. 2006;17(11):3223–32.

    Article  PubMed  Google Scholar 

  14. Fried LF, Biggs ML, Shlipak MG, Seliger S, Kestenbaum B, Stehman-Breen C, et al. Association of kidney function with incident hip fracture in older adults. J Am Soc Nephrol. 2007;18(1):282–6.

    Article  PubMed  Google Scholar 

  15. Ball AM, Gillen DL, Sherrard D, Weiss NS, Emerson SS, Seliger SL, et al. Risk of hip fracture among dialysis and renal transplant recipients. JAMA. 2002;288(23):3014–8.

    Article  PubMed  Google Scholar 

  16. Dooley AC, Weiss NS, Kestenbaum B. Increased risk of hip fracture among men with CKD. Am J Kidney Dis. 2008;51(1):38–44.

    Article  CAS  PubMed  Google Scholar 

  17. Naylor KL, McArthur E, Leslie WD, Fraser LA, Jamal SA, Cadarette SM, et al. The three-year incidence of fracture in chronic kidney disease. Kidney Int. 2014;86(4):810–8.

    Article  PubMed  Google Scholar 

  18. Isakova T, Craven TE, Scialla JJ, Nickolas TL, Schnall A, Barzilay J, et al. Change in estimated glomerular filtration rate and fracture risk in the action to control cardiovascular risk in diabetes trial. Bone. 2015;78:23–7.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ensrud KE, Lui LY, Taylor BC, Ishani A, Shlipak MG, Stone KL, et al. Renal function and risk of hip and vertebral fractures in older women. Arch Intern Med. 2007;167(2):133–9.

    Article  PubMed  Google Scholar 

  20. Nitsch D, Mylne A, Roderick PJ, Smeeth L, Hubbard R, Fletcher A. Chronic kidney disease and hip fracture-related mortality in older people in the UK. Nephrol Dial Transplant. 2009;24(5):1539–44.

    Article  PubMed  Google Scholar 

  21. Alem AM, Sherrard DJ, Gillen DL, Weiss NS, Beresford SA, Heckbert SR, et al. Increased risk of hip fracture among patients with end-stage renal disease. Kidney Int. 2000;58(1):396–9.

    Article  CAS  PubMed  Google Scholar 

  22. Maravic M, Ostertag A, Torres PU, Cohen-Solal M. Incidence and risk factors for hip fractures in dialysis patients. Osteoporos Int. 2014;25(1):159–65.

    Article  CAS  PubMed  Google Scholar 

  23. Naylor KL, Jamal SA, Zou G, McArthur E, Lam NN, Leslie WD, et al. Fracture incidence in adult kidney transplant recipients. Transplantation. 2016;100(1):167–75.

    Article  CAS  PubMed  Google Scholar 

  24. Sernbo I, Johnell O. Consequences of a hip fracture: a prospective study over 1 year. Osteoporos Int. 1993;3(3):148–53.

    Article  CAS  PubMed  Google Scholar 

  25. Kim SM, Long J, Montez-Rath M, Leonard M, Chertow GM. Hip fracture in patients with non-dialysis-requiring chronic kidney disease. J Bone Miner Res. 2016;31(10):1803–9.

    Article  PubMed  Google Scholar 

  26. Coco M, Rush H. Increased incidence of hip fractures in dialysis patients with low serum parathyroid hormone. Am J Kidney Dis. 2000;36(6):1115–21.

    Article  CAS  PubMed  Google Scholar 

  27. Beaubrun AC, Kilpatrick RD, Freburger JK, Bradbury BD, Wang L, Brookhart MA. Temporal trends in fracture rates and postdischarge outcomes among hemodialysis patients. J Am Soc Nephrol. 2013;24(9):1461–9.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Denburg M, Nickolas TL. Declining hip fracture rates in dialysis patients: is this winning the war? Am J Kidney Dis. 2018;71(2):154–6.

    Article  PubMed  Google Scholar 

  29. Sharma AK, Toussaint ND, Masterson R, Holt SG, Rajapakse CS, Ebeling PR, et al. Deterioration of cortical bone microarchitecture: critical component of renal osteodystrophy evaluation. Am J Nephrol. 2018;47(6):376–84.

    Article  CAS  PubMed  Google Scholar 

  30. Lima F, El-Husseini A, Monier-Faugere MC, David V, Mawad H, Quarles D, et al. FGF-23 serum levels and bone histomorphometric results in adult patients with chronic kidney disease on dialysis. Clin Nephrol. 2014;82(5):287–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. •• Graciolli FG, Neves KR, Barreto F, Barreto DV, Dos Reis LM, Canziani ME, et al. The complexity of chronic kidney disease-mineral and bone disorder across stages of chronic kidney disease. Kidney Int. 2017;91(6):1436–46 This study analyzed bone expression of several bone proteins, including FGF23 and sclerostin, in biopsies from healthy patients and patients with CKD 2–5 as well as bone remodeling markers. The main findings were that distinct osteocyte populations produce FGF23 and Sclerostin in ROD.

    Article  CAS  Google Scholar 

  32. • Keronen S, Martola L, Finne P, Burton IS, Kroger H, Honkanen E. Changes in bone Histomorphometry after kidney transplantation. Clin J Am Soc Nephrol. 2019;14(6):894–903 This article shows the lack of relationship between bone mineral density and bone biomarkers and bone metabolism changes.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  33. Newman CL, Chen NX, Smith E, Smith M, Brown D, Moe SM, et al. Compromised vertebral structural and mechanical properties associated with progressive kidney disease and the effects of traditional pharmacological interventions. Bone. 2015;77:50–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. McNerny EMB, Buening DT, Aref MW, Chen NX, Moe SM, Allen MR. Time course of rapid bone loss and cortical porosity formation observed by longitudinal muCT in a rat model of CKD. Bone. 2019;125:16–24.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Iwasaki Y, Kazama JJ, Yamato H, Matsugaki A, Nakano T, Fukagawa M. Altered material properties are responsible for bone fragility in rats with chronic kidney injury. Bone. 2015;81:247–54.

    Article  PubMed  Google Scholar 

  36. • Ketteler M, Block GA, Evenepoel P, Fukagawa M, Herzog CA, McCann L, et al. Executive summary of the 2017 KDIGO Chronic Kidney Disease-Mineral and Bone Disorder (CKD-MBD) Guideline update: what’s changed and why it matters. Kidney Int. 2017;92(1):26–36 This summarizes updates in KDIGO guidelines from the initial 2009 guidelines.

    Article  Google Scholar 

  37. Wilson LM, Rebholz CM, Jirru E, Liu MC, Zhang A, Gayleard J, et al. Benefits and harms of osteoporosis medications in patients with chronic kidney disease: a systematic review and meta-analysis. Ann Intern Med. 2017;166(9):649–58.

    Article  PubMed  Google Scholar 

  38. Jorgensen HS, Winther S, Bottcher M, Hauge EM, Rejnmark L, Svensson M, et al. Bone turnover markers are associated with bone density, but not with fracture in end stage kidney disease: a cross-sectional study. BMC Nephrol. 2017;18(1):284.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  39. •• Santos MFP, Hernandez MJ, de Oliveira IB, Siqueira FR, Dominguez WV, Dos Reis LM, et al. Comparison of clinical, biochemical and histomorphometric analysis of bone biopsies in dialysis patients with and without fractures. J Bone Miner Metab. 2019;37(1):125–33 This study shows increased fracture prevalence in patients with ROD and reduced cortical bone DMP1 expression, suggesting that production and secretion of this protein in ROD is of utmost significance.

    Article  CAS  PubMed  Google Scholar 

  40. Sprague SM, Bellorin-Font E, Jorgetti V, Carvalho AB, Malluche HH, Ferreira A, et al. Diagnostic accuracy of bone turnover markers and bone histology in patients with CKD treated by dialysis. Am J Kidney Dis. 2016;67(4):559–66.

    Article  PubMed  Google Scholar 

  41. Marques ID, Araujo MJ, Graciolli FG, Reis LM, Pereira RM, Custodio MR, et al. Biopsy vs. peripheral computed tomography to assess bone disease in CKD patients on dialysis: differences and similarities. Osteoporos Int. 2017;28(5):1675–83.

    Article  CAS  PubMed  Google Scholar 

  42. Salam S, Gallagher O, Gossiel F, Paggiosi M, Khwaja A, Eastell R. Diagnostic accuracy of biomarkers and imaging for bone turnover in renal osteodystrophy. J Am Soc Nephrol. 2018;29(5):1557–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. •• Nickolas TL. The quest for better biomarkers of bone turnover in CKD. J Am Soc Nephrol. 2018;29(5):1353–5 This review emphasizes the lack of definition of bone status and turnover by the existing serum biomarkers.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Gosmanova EO, Gosmanov AR. Novel approaches for assessment of bone turnover in CKD: is new always better? J Am Soc Nephrol. 2018;29(9):2443.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Ferrari GO, Ferreira JC, Cavallari RT, Neves KR, dos Reis LM, Dominguez WV, et al. Mineral bone disorder in chronic kidney disease: head-to-head comparison of the 5/6 nephrectomy and adenine models. BMC Nephrol. 2014;15:69.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  46. Christov M, Clark AR, Corbin B, Hakroush S, Rhee EP, Saito H, et al. Inducible podocyte-specific deletion of CTCF drives progressive kidney disease and bone abnormalities. JCI insight. 2018;3(4).

  47. Tani T, Orimo H, Shimizu A, Tsuruoka S. Development of a novel chronic kidney disease mouse model to evaluate the progression of hyperphosphatemia and associated mineral bone disease. Sci Rep. 2017;7(1):2233.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  48. Frauscher B, Artinger K, Kirsch AH, Aringer I, Moschovaki-Filippidou F, Ketszeri M, et al. A new murine model of chronic kidney disease-mineral and bone disorder. Int J Endocrinol. 2017;2017:1659071.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  49. Moe SM, Chen NX, Seifert MF, Sinders RM, Duan D, Chen X, et al. A rat model of chronic kidney disease-mineral bone disorder. Kidney Int. 2009;75(2):176–84.

    Article  CAS  PubMed  Google Scholar 

  50. Carrillo-Lopez N, Panizo S, Alonso-Montes C, Martinez-Arias L, Avello N, Sosa P, et al. High-serum phosphate and parathyroid hormone distinctly regulate bone loss and vascular calcification in experimental chronic kidney disease. Nephrol Dial Transplant. 2019;34(6):934–41.

    Article  PubMed  CAS  Google Scholar 

  51. Sun N, Guo Y, Liu W, Densmore M, Shalhoub V, Erben RG, et al. FGF23 neutralization improves bone quality and osseointegration of titanium implants in chronic kidney disease mice. Sci Rep. 2015;5:8304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Andrukhova O, Schuler C, Bergow C, Petric A, Erben RG. Augmented fibroblast growth factor-23 secretion in bone locally contributes to impaired bone mineralization in chronic kidney disease in mice. Front Endocrinol. 2018;9:311.

    Article  Google Scholar 

  53. de Oliveira RB, Graciolli FG, dos Reis LM, Cancela AL, Cuppari L, Canziani ME, et al. Disturbances of Wnt/beta-catenin pathway and energy metabolism in early CKD: effect of phosphate binders. Nephrol Dial Transplant. 2013;28(10):2510–7.

    Article  PubMed  CAS  Google Scholar 

  54. Lima F, Mawad H, El-Husseini AA, Davenport DL, Malluche HH. Serum bone markers in ROD patients across the spectrum of decreases in GFR: Activin A increases before all other markers. Clin Nephrol. 2019;91(4):222–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Ferreira JC, Ferrari GO, Neves KR, Cavallari RT, Dominguez WV, Dos Reis LM, Graciolli FG, Oliveira EC, Liu S, Sabbagh Y, Jorgetti V, Schiavi S, Moysés RM Effects of dietary phosphate on adynamic bone disease in rats with chronic kidney disease--role of sclerostin? PLoS One 2013;8(11):e79721.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  56. Moe SM, Chen NX, Newman CL, Organ JM, Kneissel M, Kramer I, et al. Anti-sclerostin antibody treatment in a rat model of progressive renal osteodystrophy. J Bone Miner Res. 2015;30(3):499–509.

    Article  PubMed  CAS  Google Scholar 

  57. Kaesler N, Verhulst A, De Mare A, Deck A, Behets GJ, Hyusein A, et al. Sclerostin deficiency modifies the development of CKD-MBD in mice. Bone. 2018;107:115–23.

    Article  CAS  PubMed  Google Scholar 

  58. Williams MJ, Sugatani T, Agapova OA, Fang Y, Gaut JP, Faugere MC, et al. The activin receptor is stimulated in the skeleton, vasculature, heart, and kidney during chronic kidney disease. Kidney Int. 2018;93(1):147–58.

    Article  CAS  PubMed  Google Scholar 

  59. Sugatani T, Agapova OA, Fang Y, Berman AG, Wallace JM, Malluche HH, et al. Ligand trap of the activin receptor type IIA inhibits osteoclast stimulation of bone remodeling in diabetic mice with chronic kidney disease. Kidney Int. 2017;91(1):86–95.

    Article  CAS  PubMed  Google Scholar 

  60. Cejka D, Parada-Rodriguez D, Pichler S, Marculescu R, Kramer I, Kneissel M, et al. Only minor differences in renal osteodystrophy features between wild-type and sclerostin knockout mice with chronic kidney disease. Kidney Int. 2016;90(4):828–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Fang Y, Ginsberg C, Seifert M, Agapova O, Sugatani T, Register TC, et al. CKD-induced wingless/integration1 inhibitors and phosphorus cause the CKD-mineral and bone disorder. J Am Soc Nephrol. 2014;25(8):1760–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Della Bella E, Pagani S, Giavaresi G, Capelli I, Comai G, Donadei C, et al. Uremic serum impairs osteogenic differentiation of human bone marrow mesenchymal stromal cells. J Cell Physiol. 2017;232(8):2201–9.

    Article  CAS  PubMed  Google Scholar 

  63. •• Aleksinskaya MA, Monge M, Siebelt M, Slot EM, Koekkoek KM, de Bruin RG, et al. Chronic kidney failure mineral bone disorder leads to a permanent loss of hematopoietic stem cells through dysfunction of the stem cell niche. Sci Rep. 2018;8(1):15385 This study shows profound changes in hematopoietic stem cell (HSC) niche in CKD and suggests that permanent changes in HSC might explain the loss of homeostatic potential in CKD.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  64. Martin A, Liu S, David V, Li H, Karydis A, Feng JQ, et al. Bone proteins PHEX and DMP1 regulate fibroblastic growth factor Fgf23 expression in osteocytes through a common pathway involving FGF receptor (FGFR) signaling. FASEB J. 2011;25(8):2551–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Dai B, David V, Martin A, Huang J, Li H, Jiao Y, et al. A comparative transcriptome analysis identifying FGF23 regulated genes in the kidney of a mouse CKD model. PLoS One. 2012;7(9):e44161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Portale AA, Zhang MY, David V, Martin A, Jiao Y, Gu W, et al. Characterization of FGF23-dependent Egr-1 cistrome in the mouse renal proximal tubule. PLoS One. 2015;10(11):e0142924.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  67. • Khayal LA, Grunhagen J, Provaznik I, Mundlos S, Kornak U, Robinson PN, et al. Transcriptional profiling of murine osteoblast differentiation based on RNA-seq expression analyses. Bone. 2018;113:29–40 This study analyzed the transcriptomic profile of differentiated murine primary calvaria osteoblasts and defined the key genetic regulatory mechanisms of osteoblast differentiation.

    Article  CAS  PubMed  Google Scholar 

  68. • Luttrell LM, Dar MS, Gesty-Palmer D, El-Shewy HM, Robinson KM, Haycraft CJ, et al. Transcriptomic characterization of signaling pathways associated with osteoblastic differentiation of MC-3T3E1 cells. PLoS One. 2019;14(1):e0204197 This article identified the signaling pathways involved in the differentiation of the murine osteoblastic cell line MC3T3-E1, based on the temporal sequence of changes in gene expression profiles.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Matthews BG, Roguljic H, Franceschetti T, Roeder E, Matic I, Vidovic I, et al. Gene-expression analysis of cementoblasts and osteoblasts. J Periodontal Res. 2016;51(3):304–12.

    Article  CAS  PubMed  Google Scholar 

  70. Picelli S, Faridani OR, Bjorklund AK, Winberg G, Sagasser S, Sandberg R. Full-length RNA-seq from single cells using smart-seq2. Nat Protoc. 2014;9(1):171–81.

    Article  CAS  PubMed  Google Scholar 

  71. •• Debnath S, Yallowitz AR, McCormick J, Lalani S, Zhang T, Xu R, et al. Discovery of a periosteal stem cell mediating intramembranous bone formation. Nature. 2018;562(7725):133–9 This study identified several subsets of periosteal stem cells, and defined one specific cell population involved in intramembranous bone formation.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. • Liu S, Stroncek DF, Zhao Y, Chen V, Shi R, Chen J, et al. Single cell sequencing reveals gene expression signatures associated with bone marrow stromal cell subpopulations and time in culture. Journal of translational medicine. 2019;17(1):23 This study of single cell RNA sequencing analyses of early passage bone marrow stromal cells, highlights cell heterogeneity and identified a subpopulation of cells expressing high levels of fibroblast growth factor receptor 2.

  73. Wolock SL, Krishnan I, Tenen DE, Matkins V, Camacho V, Patel S, et al. Mapping distinct bone marrow niche populations and their differentiation paths. Cell Rep. 2019;28(2):302–11 e5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Lake BB, Ai R, Kaeser GE, Salathia NS, Yung YC, Liu R, et al. Neuronal subtypes and diversity revealed by single-nucleus RNA sequencing of the human brain. Science (New York, NY). 2016;352(6293):1586–90.

    Article  CAS  Google Scholar 

  75. Habib N, Li Y, Heidenreich M, Swiech L, Avraham-Davidi I, Trombetta JJ, et al. Div-Seq: single-nucleus RNA-Seq reveals dynamics of rare adult newborn neurons. Science (New York, NY). 2016;353(6302):925–8.

    Article  CAS  Google Scholar 

  76. Nichterwitz S, Chen G, Aguila Benitez J, Yilmaz M, Storvall H, Cao M, et al. Laser capture microscopy coupled with smart-seq2 for precise spatial transcriptomic profiling. Nat Commun. 2016;7:12139.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Ayturk UM, Jacobsen CM, Christodoulou DC, Gorham J, Seidman JG, Seidman CE, et al. An RNA-seq protocol to identify mRNA expression changes in mouse diaphyseal bone: applications in mice with bone property altering Lrp5 mutations. J Bone Miner Res. 2013;28(10):2081–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was supported by grants from National Institute of Health to AM (R01DK101730) and VD (R01DK102815, R01DK114158).

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Correspondence to Aline Martin or Valentin David.

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Martin, A., David, V. Transcriptomics: a Solution for Renal Osteodystrophy?. Curr Osteoporos Rep 18, 254–261 (2020). https://doi.org/10.1007/s11914-020-00583-6

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