Colony-stimulating factor-1 promotes kidney growth and repair via alteration of macrophage responses

Maliha A Alikhan; Christina V Jones; Timothy M Williams; Anthony G Beckhouse; Anne L Fletcher; Michelle M Kett; Samy Sakkal; Chrishan S Samuel; Robert G Ramsay; James A Deane; Christine A Wells; Melissa H Little; David A Hume; Sharon D Ricardo

doi:10.1016/j.ajpath.2011.05.037

Colony-stimulating factor-1 promotes kidney growth and repair via alteration of macrophage responses

Maliha A Alikhan, Christina V Jones, Timothy M Williams, Anthony G Beckhouse, Anne L Fletcher, Michelle M Kett, Samy Sakkal, Chrishan S Samuel, Robert G Ramsay, James A Deane, Christine A Wells, Melissa H Little, David A Hume, Sharon D Ricardo

Immunology and Immunotherapy

Research output: Contribution to journal › Article › peer-review

106 Citations (Scopus)

Abstract

Colony-stimulating factor (CSF)-1 controls the survival, proliferation, and differentiation of macrophages, which are recognized as scavengers and agents of the innate and the acquired immune systems. Because of their plasticity, macrophages are endowed with many other essential roles during development and tissue homeostasis. We present evidence that CSF-1 plays an important trophic role in postnatal organ growth and kidney repair. Notably, the injection of CSF-1 postnatally enhanced kidney weight and volume and was associated with increased numbers of tissue macrophages. Moreover, CSF-1 promotes postnatal renal repair in mice after ischemia-reperfusion injury by recruiting and influencing macrophages toward a reparative state. CSF-1 treatment rapidly accelerated renal repair with tubular epithelial cell replacement, attenuation of interstitial fibrosis, and functional recovery. Analysis of macrophages from CSF-1-treated kidneys showed increased expression of insulin-like growth factor-1 and anti-inflammatory genes that are known CSF-1 targets. Taken together, these data suggest that CSF-1 is important in kidney growth and the promotion of endogenous repair and resolution of inflammatory injury.

Original language	English
Pages (from-to)	1243-56
Number of pages	14
Journal	The American Journal of Pathology
Volume	179
Issue number	3
DOIs	https://doi.org/10.1016/j.ajpath.2011.05.037
Publication status	Published - Sept 2011

Keywords

Acute Kidney Injury
Animals
Animals, Newborn
Body Weight
Cell Differentiation
Cell Proliferation
Cell Survival
Cells, Cultured
Collagen
Gene Expression Profiling
Kidney
Macrophage Colony-Stimulating Factor
Macrophages
Male
Mice
Mice, Inbred C57BL
Mice, Transgenic
Organ Size
Phenotype
Recovery of Function
Reperfusion Injury

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10.1016/j.ajpath.2011.05.037

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Alikhan, M. A., Jones, C. V., Williams, T. M., Beckhouse, A. G., Fletcher, A. L., Kett, M. M., Sakkal, S., Samuel, C. S., Ramsay, R. G., Deane, J. A., Wells, C. A., Little, M. H., Hume, D. A., & Ricardo, S. D. (2011). Colony-stimulating factor-1 promotes kidney growth and repair via alteration of macrophage responses. The American Journal of Pathology, 179(3), 1243-56. https://doi.org/10.1016/j.ajpath.2011.05.037

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title = "Colony-stimulating factor-1 promotes kidney growth and repair via alteration of macrophage responses",

abstract = "Colony-stimulating factor (CSF)-1 controls the survival, proliferation, and differentiation of macrophages, which are recognized as scavengers and agents of the innate and the acquired immune systems. Because of their plasticity, macrophages are endowed with many other essential roles during development and tissue homeostasis. We present evidence that CSF-1 plays an important trophic role in postnatal organ growth and kidney repair. Notably, the injection of CSF-1 postnatally enhanced kidney weight and volume and was associated with increased numbers of tissue macrophages. Moreover, CSF-1 promotes postnatal renal repair in mice after ischemia-reperfusion injury by recruiting and influencing macrophages toward a reparative state. CSF-1 treatment rapidly accelerated renal repair with tubular epithelial cell replacement, attenuation of interstitial fibrosis, and functional recovery. Analysis of macrophages from CSF-1-treated kidneys showed increased expression of insulin-like growth factor-1 and anti-inflammatory genes that are known CSF-1 targets. Taken together, these data suggest that CSF-1 is important in kidney growth and the promotion of endogenous repair and resolution of inflammatory injury.",

keywords = "Acute Kidney Injury, Animals, Animals, Newborn, Body Weight, Cell Differentiation, Cell Proliferation, Cell Survival, Cells, Cultured, Collagen, Gene Expression Profiling, Kidney, Macrophage Colony-Stimulating Factor, Macrophages, Male, Mice, Mice, Inbred C57BL, Mice, Transgenic, Organ Size, Phenotype, Recovery of Function, Reperfusion Injury",

author = "Alikhan, {Maliha A} and Jones, {Christina V} and Williams, {Timothy M} and Beckhouse, {Anthony G} and Fletcher, {Anne L} and Kett, {Michelle M} and Samy Sakkal and Samuel, {Chrishan S} and Ramsay, {Robert G} and Deane, {James A} and Wells, {Christine A} and Little, {Melissa H} and Hume, {David A} and Ricardo, {Sharon D}",

year = "2011",

month = sep,

doi = "10.1016/j.ajpath.2011.05.037",

language = "English",

volume = "179",

pages = "1243--56",

journal = "The American Journal of Pathology",

issn = "0002-9440",

publisher = "American Society for Investigative Pathology",

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Alikhan, MA, Jones, CV, Williams, TM, Beckhouse, AG, Fletcher, AL, Kett, MM, Sakkal, S, Samuel, CS, Ramsay, RG, Deane, JA, Wells, CA, Little, MH, Hume, DA & Ricardo, SD 2011, 'Colony-stimulating factor-1 promotes kidney growth and repair via alteration of macrophage responses', The American Journal of Pathology, vol. 179, no. 3, pp. 1243-56. https://doi.org/10.1016/j.ajpath.2011.05.037

TY - JOUR

T1 - Colony-stimulating factor-1 promotes kidney growth and repair via alteration of macrophage responses

AU - Alikhan, Maliha A

AU - Jones, Christina V

AU - Williams, Timothy M

AU - Beckhouse, Anthony G

AU - Fletcher, Anne L

AU - Kett, Michelle M

AU - Sakkal, Samy

AU - Samuel, Chrishan S

AU - Ramsay, Robert G

AU - Deane, James A

AU - Wells, Christine A

AU - Little, Melissa H

AU - Hume, David A

AU - Ricardo, Sharon D

PY - 2011/9

Y1 - 2011/9

N2 - Colony-stimulating factor (CSF)-1 controls the survival, proliferation, and differentiation of macrophages, which are recognized as scavengers and agents of the innate and the acquired immune systems. Because of their plasticity, macrophages are endowed with many other essential roles during development and tissue homeostasis. We present evidence that CSF-1 plays an important trophic role in postnatal organ growth and kidney repair. Notably, the injection of CSF-1 postnatally enhanced kidney weight and volume and was associated with increased numbers of tissue macrophages. Moreover, CSF-1 promotes postnatal renal repair in mice after ischemia-reperfusion injury by recruiting and influencing macrophages toward a reparative state. CSF-1 treatment rapidly accelerated renal repair with tubular epithelial cell replacement, attenuation of interstitial fibrosis, and functional recovery. Analysis of macrophages from CSF-1-treated kidneys showed increased expression of insulin-like growth factor-1 and anti-inflammatory genes that are known CSF-1 targets. Taken together, these data suggest that CSF-1 is important in kidney growth and the promotion of endogenous repair and resolution of inflammatory injury.

AB - Colony-stimulating factor (CSF)-1 controls the survival, proliferation, and differentiation of macrophages, which are recognized as scavengers and agents of the innate and the acquired immune systems. Because of their plasticity, macrophages are endowed with many other essential roles during development and tissue homeostasis. We present evidence that CSF-1 plays an important trophic role in postnatal organ growth and kidney repair. Notably, the injection of CSF-1 postnatally enhanced kidney weight and volume and was associated with increased numbers of tissue macrophages. Moreover, CSF-1 promotes postnatal renal repair in mice after ischemia-reperfusion injury by recruiting and influencing macrophages toward a reparative state. CSF-1 treatment rapidly accelerated renal repair with tubular epithelial cell replacement, attenuation of interstitial fibrosis, and functional recovery. Analysis of macrophages from CSF-1-treated kidneys showed increased expression of insulin-like growth factor-1 and anti-inflammatory genes that are known CSF-1 targets. Taken together, these data suggest that CSF-1 is important in kidney growth and the promotion of endogenous repair and resolution of inflammatory injury.

KW - Acute Kidney Injury

KW - Animals

KW - Animals, Newborn

KW - Body Weight

KW - Cell Differentiation

KW - Cell Proliferation

KW - Cell Survival

KW - Cells, Cultured

KW - Collagen

KW - Gene Expression Profiling

KW - Kidney

KW - Macrophage Colony-Stimulating Factor

KW - Macrophages

KW - Male

KW - Mice

KW - Mice, Inbred C57BL

KW - Mice, Transgenic

KW - Organ Size

KW - Phenotype

KW - Recovery of Function

KW - Reperfusion Injury

U2 - 10.1016/j.ajpath.2011.05.037

DO - 10.1016/j.ajpath.2011.05.037

M3 - Article

C2 - 21762674

SN - 0002-9440

VL - 179

SP - 1243

EP - 1256

JO - The American Journal of Pathology

JF - The American Journal of Pathology

IS - 3

ER -

Colony-stimulating factor-1 promotes kidney growth and repair via alteration of macrophage responses

Abstract

Keywords

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