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A novel form of ciliopathy underlies hyperphagia and obesity in Ankrd26 knockout mice

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Abstract

Human ciliopathies are genetic disorders caused by mutations in genes responsible for the formation and function of primary cilia. Some are associated with hyperphagia and obesity (e.g., Bardet–Biedl Syndrome, Alström Syndrome), but the mechanisms underlying these problems are not fully understood. The human gene ANKRD26 is located on 10p12, a locus that is associated with some forms of hereditary obesity. Previously, we reported that disruption of this gene causes hyperphagia, obesity and gigantism in mice. In the present study, we looked for the mechanisms that induce hyperphagia in the Ankrd26−/− mice and found defects in primary cilia in regions of the central nervous system that control appetite and energy homeostasis.

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Abbreviations

AC3:

Adenylyl cyclase 3

ACTH:

Adrenocorticotrophic hormone

ADX:

Adrenalectomy

α-MSH:

α-Melanocyte stimulating hormone

AgRP:

Agouti-related protein

Ankrd26:

Ankyrin repeat domain 26

ARC:

Arcuate nucleus

BBS:

Bardet–Biedl syndrome

BW:

Body weight

CNS:

Central nervous system

CORT:

Corticosterone

CRH:

Corticotropin-releasing hormone

DM:

Dorsomedial nucleus of the hypothalamus

GPCR:

G-protein-coupled receptor

HPA:

Hypothalamus–pituitary–adrenal

IHC:

Immunohistochemistry

MC4R:

Melanocortin 4 receptor

Mchr1:

Melanin-concentrating hormone receptor 1

NPY:

Neuropeptide Y

NTS:

Nucleus of the solitary tract

POMC:

Proopiomelanocortin

PVN:

Paraventricular nucleus of the hypothalamus

Sstr3:

Somatostatin receptor 3

TRH:

Thyrotropin releasing hormone

VM:

Ventromedial nucleus of the hypothalamus

VP:

Arginine vasopressin

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Acknowledgments

The authors want to acknowledge the invaluable help of Miklos Palkovits, Harold Gainer and Michael Brownstein for their continuous support and advice as well as help with editing the manuscript. We also thank Prof. Ronald DeKloet (Leiden University) for his expert advice regarding studies on adrenal function. This research was supported by the Division of Intramural Research program of NCI and NIDCR in the Intramural Research Program, NIH, DHHS. We dedicate this work to the memory of Wylie Vale, who discovered CRF and who was an outstanding scientist; a wonderful human being and a good friend.

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Authors and Affiliations

  1. Laboratory of Molecular Biology, National Cancer Institute, NIH, Bethesda, USA

    Peter Acs, Tapan Bera & Ira Pastan

  2. Neuro-oncology Branch, National Cancer Institute, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, USA

    Peter O. Bauer

  3. Adult Stem Cell Unit, CSDB, National Institute of Dental and Craniofacial Research, NIH, Bethesda, USA

    Balazs Mayer & Eva Mezey

  4. National Cancer Institute, NIH, Bethesda, USA

    Rhonda Macallister

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  1. Peter Acs
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  2. Peter O. Bauer
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  3. Balazs Mayer
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  4. Tapan Bera
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  6. Eva Mezey
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  7. Ira Pastan
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Corresponding author

Correspondence to Eva Mezey.

Additional information

E. Mezey and I. Pastan contributed equally to the work.

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429_2014_741_MOESM1_ESM.jpg

Combination of immunohistochemistry and in situ hybridization to show specificity of the antibodies used. Leptin receptor (LeptinR) and melanocortin receptor 4 (MC4R) mRNA were detected using specific probes and the RNAScope technique (Advanced Cell Diagnostics) according to the company’s protocol. Following detection of the specific mRNAs (red color), immunostaining was performed as described in the methods, using the TSA amplification technique and a Tyramide-680 Plus substrate (yellow color). The significant overlap between the labelings indicates that the immunostaining is indeed specific for the two receptors. (JPEG 663 kb)

429_2014_741_MOESM2_ESM.tif

Expression of rootletin in WT and Ankrd − / − mice. IHC for rootletin in the CA3 region of the hippocampus in WT (A and B) and in Ankrd26−/− (C and D) mice. Note that the stronger cytoplasmic signal is accompanied by apparent ciliary rootlets (indicated by arrows) in Ankrd26−/− mice. Nuclei are visualized with Dapi (blue). Scale bar: 15 μm. Images are representative of four independent observations (n = 3 in each group, four different litters). (TIFF 9527 kb)

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Acs, P., Bauer, P.O., Mayer, B. et al. A novel form of ciliopathy underlies hyperphagia and obesity in Ankrd26 knockout mice. Brain Struct Funct 220, 1511–1528 (2015). https://doi.org/10.1007/s00429-014-0741-9

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