Novel in vivo techniques to visualize kidney anatomy and function

Kidney International

Volumn 88, Issue 1, 2015, Pages 44-51

  Peti Peterdi, János ^a   Kidokoro, Kengo ^a,b   Riquier Brison, Anne ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b KAWASAKI MEDICAL SCHOOL   (Japan)

Author keywords

Glomerulus; Intracellular calcium; Intravital imaging; Multiphoton microscopy; Podocyte

Indexed keywords

ANATOMICAL CONCEPTS; ARTICLE; BOWMAN CAPSULE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL FATE; CELL LINEAGE; DISEASE COURSE; FOCAL GLOMERULOSCLEROSIS; GLOMERULAR FILTRATION BARRIER; GLOMERULOPATHY; GLOMERULUS; GLOMERULUS FILTRATION; GLOMERULUS FILTRATION RATE; IN VIVO STUDY; KIDNEY BLOOD FLOW; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY PARENCHYMA; MICROMANIPULATION; MULTIPHOTON MICROSCOPY; NEPHRON; NONHUMAN; OSCILLATION; PODOCYTE; PRIORITY JOURNAL; TIME LAPSE IMAGING; TRANSGENICS; ANATOMY AND HISTOLOGY; ANIMAL; CELL MOTION; INTRAVITAL MICROSCOPY; KIDNEY DISEASE; METABOLISM; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; RAT; ZEBRA FISH;

CALCIUM;

ANIMALS; CALCIUM; CELL MOVEMENT; GLOMERULAR FILTRATION BARRIER; INTRAVITAL MICROSCOPY; KIDNEY DISEASES; MICE; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; PODOCYTES; RATS; TIME-LAPSE IMAGING; ZEBRAFISH;

EID: 84934441012     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2015.65     Document Type: Review

References (69)

1. Mundel P, Kriz W. Structure and function of podocytes: an update. Anat Embryol 1995; 192: 385-397.
2. Mundel P, Reiser J, Kriz W. Induction of differentiation in cultured rat and human podocytes. J Am Soc Nephrol 1997; 8: 697-705.
3. Nitschke R, Henger A, Ricken S et al. Angiotensin II increases the intracellular calcium activity in podocytes of the intact glomerulus. Kidney Int 2000; 57: 41-49.
4. Dunn KW, Young PA. Principles of multiphoton microscopy. Nephron Exp Nephrol 2006; 103: e33-e40.
5. Hall AM, Molitoris BA. Dynamic multiphoton microscopy: focusing light on acute kidney injury. Physiology 2014; 29: 334-342.
6. Kang JJ, Toma I, Sipos A et al. Quantitative imaging of basic functions in renal (patho)physiology. Am J Physiol Renal Physiol 2006; 291: F495-F502.
7. Peti-Peterdi J, Burford JL, Hackl MJ. The first decade of using multiphoton microscopy for high-power kidney imaging. Am J Physiol Renal Physiol 2012; 302: F227-F233.
8. Peti-Peterdi J, Toma I, Sipos A et al. Multiphoton imaging of renal regulatory mechanisms. Physiology 2009; 24: 88-96.
9. Sipos A, Toma I, Kang JJ et al. Advances in renal (patho)physiology using multiphoton microscopy. Kidney Int 2007; 72: 1188-1191.
10. Molitoris BA, Sandoval RM. Intravital multiphoton microscopy of dynamic renal processes. Am J Physiol Renal Physiol 2005; 288: F1084-F1089.
11. Peti-Peterdi J. Multiphoton imaging of renal tissues in vitro. Am J Physiol Renal Physiol 2005; 288: F1079-F1083.
12. Peti-Peterdi J, Morishima S, Bell PD et al. Two-photon excitation fluorescence imaging of the living juxtaglomerular apparatus. Am J Physiol Renal Physiol 2002; 283: F197-F201.
13. Dunn KW, Sandoval RM, Kelly KJ et al. Functional studies of the kidney of living animals using multicolor two-photon microscopy. Am J Physiol Cell Physiol 2002; 283: C905-C916.
14. Yu W, Sandoval RM, Molitoris BA. Rapid determination of renal filtration function using an optical ratiometric imaging approach. Am J Physiol Renal Physiol 2007; 292: F1873-F1880.
15. Wang E, Meier DJ, Sandoval RM et al. A portable fiberoptic ratiometric fluorescence analyzer provides rapid point-of-care determination of glomerular filtration rate in large animals. Kidney Int 2012; 81: 112-117.
16. Nakano D, Kobori H, Burford JL et al. Multiphoton imaging of the glomerular permeability of angiotensinogen. J Am Soc Nephrol 2012; 23: 1847-1856.
17. Rosivall L, Mirzahosseini S, Toma I et al. Fluid flow in the juxtaglomerular interstitium visualized in vivo. Am J Physiol Renal Physiol 2006; 291: F1241-F1247.
18. Russo LM, Sandoval RM, McKee M et al. The normal kidney filters nephrotic levels of albumin retrieved by proximal tubule cells: retrieval is disrupted in nephrotic states. Kidney Int 2007; 71: 504-513.
19. Salmon AH, Ferguson JK, Burford JL et al. Loss of the endothelial glycocalyx links albuminuria and vascular dysfunction. J Am Soc Nephrol 2012; 23: 1339-1350.
20. Toma I, Kang JJ, Sipos A et al. Succinate receptor GPR91 provides a direct link between high glucose levels and renin release in murine and rabbit kidney. J Clin Invest 2008; 118: 2526-2534.
21. Burford JL, Villanueva K, Lam L et al. Intravital imaging of podocyte calcium in glomerular injury and disease. J Clin Invest 2014; 124: 2050-2058.
22. Svenningsen P, Burford JL, Peti-Peterdi J. ATP releasing connexin 30 hemichannels mediate flow-induced calcium signaling in the collecting duct. Front Physiol 2013; 4: 292.
23. Brasen JC, Burford JL, McDonough AA et al. Local pH domains regulate NHE3 mediated Na+ reabsorption in the renal proximal tubule. Am J Physiol Renal Physiol 2014; 307: F1249-F1262.
24. Sandoval RM, Kennedy MD, Low PS et al. Uptake and trafficking of fluorescent conjugates of folic acid in intact kidney determined using intravital two-photon microscopy. Am J Physiol Cell Physiol 2004; 287: C517-C526.
25. Hall AM, Crawford C, Unwin RJ et al. Multiphoton imaging of the functioning kidney. J Am Soc Nephrol 2011; 22: 1297-1304.
26. Hall AM, Rhodes GJ, Sandoval RM et al. In vivo multiphoton imaging of mitochondrial structure and function during acute kidney injury. Kidney Int 2013; 83: 72-83.
27. Holstein-Rathlou NH, Leyssac PP. TGF-mediated oscillations in the proximal intratubular pressure: differences between spontaneously hypertensive rats and Wistar-Kyoto rats. Acta Physiol Scand 1986; 126: 333-339.
28. Marsh DJ, Sosnovtseva OV, Chon KH et al. Nonlinear interactions in renal blood flow regulation. Am J Physiol Regul Integr Comp Physiol 2005; 288: R1143-R1159.
29. Peti-Peterdi J, Sipos A. A high-powered view of the filtration barrier. J Am Soc Nephrol 2010; 21: 1835-1841.
30. Praetorius HA, Frokiaer J, Leipziger J. Transepithelial pressure pulses induce nucleotide release in polarized MDCK cells. Am J Physiol Renal Physiol 2005; 288: F133-F141.
31. Toma I, Kang JJ, Peti-Peterdi J. Imaging renin content and release in the living kidney. Nephron Physiol 2006; 103: p71-p74.
32. Salmon AH, Toma I, Sipos A et al. Evidence for restriction of fluid and solute movement across the glomerular capillary wall by the subpodocyte space. Am J Physiol Renal Physiol 2007; 293: F1777-F1786.
33. Mundel P, Reiser J. Proteinuria: an enzymatic disease of the podocyte? Kidney Int 2010; 77: 571-580.
34. Endlich N, Simon O, Gopferich A et al. Two-photon microscopy reveals stationary podocytes in living zebrafish larvae. J Am Soc Nephrol 2014; 25: 681-686.
35. Keir L, Coward RJ. Advances in our understanding of the pathogenesis of glomerular thrombotic microangiopathy. Pediatr Nephrol 2011; 26: 523-533.
36. Schlondorff D. Putting the glomerulus back together: per aspera ad astra ("a rough road leads to the stars"). Kidney Int 2014; 85: 991-998.
37. Sandoval RM, Wagner MC, Patel M et al. Multiple factors influence glomerular albumin permeability in rats. J Am Soc Nephrol 2012; 23: 447-457.
38. Tanner GA. Glomerular sieving coefficient of serum albumin in the rat: a two-photon microscopy study. Am J Physiol Renal Physiol 2009; 296: F1258-F1265.
39. Schiessl IM, Castrop H. Angiotensin II AT2 receptor activation attenuates AT1 receptor-induced increases in the glomerular filtration of albumin: a multiphoton microscopy study. Am J Physiol Renal Physiol 2013; 305: F1189-F1200.
40. Helmchen F, Denk W. Deep tissue two-photon microscopy. Nat Methods 2005; 2: 932-940.
41. Hackl MJ, Burford JL, Villanueva K et al. Tracking the fate of glomerular epithelial cells in vivo using serial multiphoton imaging in new mouse models with fluorescent lineage tags. Nat Med 2013; 19: 1661-1666.
42. Hohne M, Ising C, Hagmann H et al. Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions. Am J Pathol 2013; 182: 332-338.
43. Khoury CC, Khayat MF, Yeo TK et al. Visualizing the mouse podocyte with multiphoton microscopy. Biochem Biophys Res Commun 2012; 427: 525-530.
44. Kistler AD, Caicedo A, Abdulreda MH et al. In vivo imaging of kidney glomeruli transplanted into the anterior chamber of the mouse eye. Sci Rep 2014; 4: 3872.
45. Vasilyev A, Liu Y, Mudumana S et al. Collective cell migration drives morphogenesis of the kidney nephron. PLoS Biol 2009; 7: e9.
46. Zhou W, Hildebrandt F. Inducible podocyte injury and proteinuria in transgenic zebrafish. J Am Soc Nephrol 2012; 23: 1039-1047.
47. Corridon PR, Rhodes GJ, Leonard EC et al. A method to facilitate and monitor expression of exogenous genes in the rat kidney using plasmid and viral vectors. Am J Physiol Renal Physiol 2013; 304: F1217-F1229.
48. Devi S, Li A, Westhorpe CL et al. Multiphoton imaging reveals a new leukocyte recruitment paradigm in the glomerulus. Nat Med 2013; 19: 107-112.
49. Schiessl IM, Bardehle S, Castrop H. Superficial nephrons in BALB/c and C57BL/6 mice facilitate in vivo multiphoton microscopy of the kidney. PLoS One 2013; 8: e52499.
50. Grgic I, Brooks CR, Hofmeister AF et al. Imaging of podocyte foot processes by fluorescence microscopy. J Am Soc Nephrol 2012; 23: 785-791.
51. Peti-Peterdi J, Burford JL, Hackl MJ. Can kidney regeneration be visualized? Nephron Exp Nephrol 2014; 126: 86.
52. Kotb AM, Muller T, Xie J et al. Simultaneous assessment of glomerular filtration and barrier function in live zebrafish. Am J Physiol Renal Physiol 2014; 307: F1427-F1434.
53. O'Connor AK, Malarkey EB, Berbari NF et al. An inducible CiliaGFP mouse model for in vivo visualization and analysis of cilia in live tissue. Cilia 2013; 2: 8.
54. Peppiatt-Wildman CM, Crawford C, Hall AM. Fluorescence imaging of intracellular calcium signals in intact kidney tissue. Nephron Exp Nephrol 2012; 121: e49-e58.
55. Gee JM, Smith NA, Fernandez FR et al. Imaging activity in neurons and glia with a Polr2a-based and cre-dependent GCaMP5G-IRES-tdTomato reporter mouse. Neuron 2014; 83: 1058-1072.
56. Dana H, Chen TW, Hu A et al. Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo. PLoS One 2014; 9: e108697.
57. Arosio D, Ratto GM. Twenty years of fluorescence imaging of intracellular chloride. Front Cell Neurosci 2014; 8: 258.
58. Bencina M. Illumination of the spatial order of intracellular pH by genetically encoded pH-sensitive sensors. Sensors 2013; 13: 16736-16758.
59. Han Z, Jin L, Chen F et al. Mechanistic studies of the genetically encoded fluorescent protein voltage probe ArcLight. PLoS One 2014; 9: e113873.
60. Ai HW. Fluorescent-protein-based probes: general principles and practices. Anal Bioanal Chem 2015; 407: 9-15.
61. Peti-Peterdi J. Calcium wave of tubuloglomerular feedback. Am J Physiol Renal Physiol 2006; 291: F473-F480.
62. Schaldecker T, Kim S, Tarabanis C et al. Inhibition of the TRPC5 ion channel protects the kidney filter. J Clin Invest 2013; 123: 5298-5309.
63. Ilatovskaya DV, Palygin O, Chubinskiy-Nadezhdin V et al. Angiotensin II has acute effects on TRPC6 channels in podocytes of freshly isolated glomeruli. Kidney Int 2014; 86: 506-514.
64. Kang S, Vora K, Shukla S et al. Femtosecond laser nanofabrication of metal structures through multiphoton photoreduction. In: Di Bartolo B, Collins J (eds). Nano-Optics for Enhancing Light-Matter Interactions on a Molecular Scale. Springer: Netherlands, 2013, pp 411-412.
65. Witte S, Negrean A, Lodder JC et al. Label-free live brain imaging and targeted patching with third-harmonic generation microscopy. Proc Natl Acad Sci USA 2011; 108: 5970-5975.
66. Croix CS, Zipfel WR, Watkins SC. Potential solutions for confocal imaging of living animals. Biotechniques 2007; 43: 14-19.
67. Xi J, Chen Y, Zhang Y et al. Integrated multimodal endomicroscopy platform for simultaneous en face optical coherence and two-photon fluorescence imaging. Opt Lett 2012; 37: 362-364.
68. Suleiman H, Zhang L, Roth R et al. Nanoscale protein architecture of the kidney glomerular basement membrane. Elife 2013; 2: e01149.
69. Tomer R, Ye L, Hsueh B et al. Advanced CLARITY for rapid and highresolution imaging of intact tissues. Nat Protoc 2014; 9: 1682-1697.