Alzheimer's Disease and Frontotemporal Dementias

	On-line Review Paper (2001) Pin1 protein: a key player in the molecular pathogenesis of AD? Thorpe JR
	Pin1 Promoter Polymorphisms, which result in decreased expression, correlate with AD (Segat et al., In Press).

Pin1 and Tangles (Includes diagram of possible involvement of Pin1 in tangle formation)

Pin1 and APP/Plaque Formation (Includes diagram of possible involvement of Pin1 in plaque formation) N.B. But please now see comment on Pastoriono et al. below

Pin1 and Cell Cycle Events in AD

	Pin1 and Apoptosis in AD (Includes diagram of possible involvement of Pin1 in apoptosis)
	Pin1 and b-catenin/Notch and Wnt Signalling in AD

Diagram of Possible Pin1 Binding Events in AD

Comments on Specific Articles

***** Comment for Alzheimer Research Forum upon ‘Pastoriono L et al. The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-b production. Nature 440: 528-534’ *****

***** Review of Nature paper by K.P. Lu and colleagues on Pin1 knockout mice *****

Pin1 protein has been shown to have an intimate involvement in the formation of the two classical hallmark histopathological features of AD, the extracellular neuritic plaques and the intraneuronal neurofibrillary tangles.

The finding that Pin1 binds to the amyloid protein precursor (APP : Davies et al., 2000 ) alongside the earlier demonstration of its binding to the microtubule-associated protein tau in the neurofibrillary tangles of AD-affected neurons ( Lu et al., 1999a ), means that the protein provides a link between the two major histopathological hallmark features of this disease, the plaques and tangles. (It is the aberrant proteolytic processing of APP that leads to the secretion and ultimate aggregation of beta-amyloid peptides into extracellular plaques in AD brain, whilst hyperphosphorylated tau is the major component of the tangles within the perikaryon of affected neurons).

Additionally, as Pin1 is a mitotic regulator , it is highly likely that the protein will have a role in the spurious expression of cell cycle-related proteins in AD which has attracted much research interest (e.g. see Husseman et al., 2000 , Vincent et al., 1996 ) and has been described as an ‘interrupted’ mitotic process which leads to associated cytoskeletal abnormalities (including tangle formation). A possible role for Pin1 in neuronal apoptosis would therefore also follow (see links below).

Comment for ARF upon ‘Pastoriono L et al. The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-b production. Nature 440: 528-534’

Julian Thorpe

KP Lu‘s group and his collaborators have been at the fore of elucidating Pin1’s cellular roles, including, since discovering that tau is a Pin1 target protein, its involvement in neurodegeneration. On the basis of their accumulated data that depletion of Pin1 causes apoptosis in HeLa cells, that patterns of AD pathology correlate with regions of lower Pin1 expression in normal human brain, that Pin1 knockout mice suffer neurodegeneration and that Pin1 can ameliorate p-tau pathology, they have suggested that a fuller elucidation of Pin1’s involvement in neurodegeneration (and cancer) might lead to new therapeutic strategies.

Our group has acquired data confirmatory of, and complementary to, that of Lu and his co-workers. We have observed Pin1 deficits in a range of frontotemporal dementias and in ageing normal brain neurons and have suggested that this might be a susceptibility factor both in neurodegenerative disease (Thorpe et al., 2004) and in ageing-related neurodegeneration (Hashemzadeh-Bonehi et al., In Press).

In this latest work, Lu and colleagues suggest that deficits of Pin1 would also be deleterious to neurons in respect of Ab secretion; it binds to p-Thr668 of APP and its overexpression reduces Ab secretion in cell cultures, whilst knockdown, both in cells and mice, selectively increases secretion of the toxic amyloid species, Ab42. A concern is that this data is contradictory to the work of others (Akiyama et al., 2005), which is not referred to in this present work. Akiyama et al. also used knockdown mice and several cell lines (different to those used by Lu et al.). I can only presume that differences in genetic background might account for the discrepant data between these two studies; although the source of the Pin1 KO mouse is the same for both groups, it appears that Lu's group maintain their colony in an inbred C57/S129 line, whereas Akiyama’s group maintain a C57/B6 strain. Clear differences have been observed in these strains’ behavioural phenotypes. Additionally, the mouse brain gene expression database shows higher hippocampal Gsk3b expression in an S129-derived strain than in a C57/B6 strain. Such strain differences, especially local concentrations of upstream APP kinases, could influence APP processing. Indeed, the elucidation of these differences might add important new insights into the neurodegenerative process.

Whilst research showing involvements of just one specific protein in molecular neuropathological pathways do not confirm their centrality to a disease, other recent research evidence is supportive of such a view: Pin1 promoter polymorphisms, which result in lowered protein expression, correlate with AD (Segat et al., In Press) and Pin1 is one of a handful of proteins susceptible to oxidation in MCI hippocampus, with the authors suggesting that this may be involved in the progression from MCI to AD (Butterfield et al., In Press). Thus, if the concern re conflicting data above is addressed, this new data from Lu’s group could put Pin1 protein potentially at the heart of the ameliorative influences that might slow or halt the key twin molecular neuropathological pathways leading to plaque and tangle formation and thence neuronal cell death in AD.

References:

Akiyama H, Shin R-W, Uchida C, Kitamtoto T, Uchida T(2005) Pin1 promotes production of Alzheimer's amyloid b from b-cleaved amyloid precursor protein. Biochemical and Biophysical Research Communications 336: 521-529

Butterfield DA, Poon HF, Clair DSt, Keller JN, Pierce WM, Klein JB, Markesbery WR (In Press) Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: Insights into the development of Alzheimer's disease. Neurobiology of Disease

Hashemzadeh-Bonehi L, Phillips RG, Cairns NJ, Mosaheb S, Thorpe JR (In Press) Pin1 protein associates with neuronal lipofuscin: potential consequences in age-related neurodegeneration. Experimental Neurology

Segat L, Pontillo A, Annoni G, Trabattoni D, Vergani C, Clerici M, Arosio B, Crovella S (In Press) Pin1 promoter polymorphisms are associated with Alzheimer's disease. Neurobiology of Aging

Thorpe JR, Mosaheb S, Hashemzadeh-Bonehi L, Cairns NJ, Kay KE, Morley SJ, Rulten S (2004) Shortfalls in the Peptidyl-Prolyl Cis-Trans Isomerase Protein Pin1 in Neurons are Associated With Frontotemporal Dementias. Neurobiology of Disease 17: 237-249

Review of Nature paper by K.P. Lu and colleagues on Pin1 knockout mice

Ref.: Liou Y-C, Sun A, Ryo A, Zhou XZ, Yu Z-X, Huang H-K, Uchida T, Bronson R, Bing G, Li X, Hunter T, Lu KP (2003) Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature 424: 556-561

(A commentary on the paper that I was asked to provide The Lancet:)

“I believe that this latest work by Lu and colleagues is potentially very significant, as it provides strong evidence that one particular protein, Pin1, may have a central role in the protection of neurons against neurodegenerative insult. This chaperone protein binds to a specific phosphorylated ‘motif’ on a range of target proteins involved in the cell cycle, transcription, translation, endocytosis and apoptosis, and thereby modulates their bioactivities; Pin1 can thus exert control over a variety of key cellular processes.

Many of Pin1’s target proteins are mitotic phosphoproteins and aberrant re-entry into the cell cycle in AD is thought by many to be the cause of the abnormal phosphorylation of neuronal cell proteins. One of these latter proteins is tau, a component of the neuronal cytoskeleton that maintains the normal function of microtubules. In AD (and other ‘tauopathies’), it becomes abnormally hyper-phosphorylated, dissociates from the microtubules and forms the so-called filamentous ‘tangles’, a neuropathological hallmark feature of the disease.

Lu and colleagues have previously shown that available, soluble Pin1 is depleted in tangle-bearing neurons of AD brain. Very importantly, they also showed that, in vitro, Pin1 could restore the ability of tau to re-associate with, and reconstitute the integrity of, the microtubules. In this latest research, their hypothesis of a potentially neuroprotective role for Pin1 has been strengthened. Not only do they show that there are lower levels of Pin1 protein in susceptible regions of normal human brain, but also that there is an inverse correlation of neuronal Pin1 and tangle content in AD-affected brain. Finally, and most notably, they have shown that aged Pin1 knockout mice have behavioural and motor deficits, neuronal loss and an accumulation of phosphorylated proteins, including tau that forms filaments and assumes a tangle-like conformation.

Overall, this work establishes Pin1 as an important protein in AD and, implicitly, the other tauopathies. Future work should also provide insights into the effects of Pin1 levels on the course of neurodegenerative disease progression through its control of transcription, translation, endocytosis and apoptosis.”

Our Pin1 Publications:

THORPE, J.R. , MORLEY, S.J. and RULTEN, S.L. (2001) (read Abstract ) Utilising the Peptidyl-Prolyl Cis-Trans Isomerase Pin1 as a Probe of its Phosphorylated Target Proteins: Examples of Binding to Nuclear Proteins in a Human Kidney Cell Line and to Tau in Alzheimer’s Diseased Brain. J. Histochem. Cytochem. 49: 97-108

THORPE, J.R. , RULTEN, S.L. and KAY, J.E. (1999) (read Abstract ) The binding of a putative and a known chaperone protein revealed by immunogold labelling transmission electron microscopy: A suggested use of chaperones as probes for the distribution of their target proteins. J. Histochem. Cytochem. 47, 1633-1640

Pin1 and Pin1-Related References

N.B. Free Medical Journals online now at: http://www.freemedicaljournals.com/
(These journals include: Neurology, Neurobiology of Disease, Journal of Neurochemistry, Alzheimer's Disease Review)

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